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CHEMOKINES
From the James Ewing Laboratory of Developmental
Hematopoiesis, Sloan-Kettering Institute for Cancer Research; Division
of Hematology-Oncology, Weill Medical College of Cornell University;
and Division of Pulmonary and Critical Care Medicine, The New York
Hospital-Cornell Medical Center, New York, NY; the Center for
Molecular Biology and Genetics, and Department of Medical Chemistry,
Faculty of Medicine, Kyoto University, Japan; and the
Department of Pathology, Sapporo City General Hospital,
Japan.
The chemokine, stromal cell-derived factor-1 (SDF1), is produced
in the bone marrow and has been shown to modulate the homing of stem
cells to this site by mediating chemokinesis and chemotaxis. Therefore,
it was hypothesized that elevation of SDF1 level in the peripheral
circulation would result in mobilization of primitive hematopoietic
stem and progenitor cells. SDF1 plasma level was increased by
intravenous injection of an adenoviral vector expressing SDF1 In adulthood, hematopoiesis is restricted to the
extravascular compartment of the bone marrow (BM) separated by a single
layer of BM endothelial cells (BMECs). Thus, hematopoietic stem cells (HSCs) arriving at the BM must first be recognized by the luminal surface of the BMEC.1-5 Molecules that mediate adhesion of
HSCs to BMECs are likely to play a pivotal role in the phenomenon of HSC homing.1-3,6-8 Similar to leukocyte
trafficking,9,10 homing of HSCs from the peripheral
circulation to the BM is a multistep process and involves sequential
interaction of CD34+ cells with adhesion molecules
expressed on BMECs, and specific chemokine(s) expressed within the BM.
Chemokines orchestrate this process by providing directional cues for
CD34+ cells to migrate into the BM microenvironment.
The chemokine, stromal cell-derived factor-1 (SDF1), which is produced
by marrow stromal cells, has been shown to play a key role in
CD34+ trafficking.11-14 Targeted gene knockout
of either SDF115 or its receptor CXCR416,17
resulted in a defect in BM hematopoiesis, whereas fetal liver
hematopoietic activity remained intact. Recently, it was shown that
transendothelial migration of primitive hematopoietic precursors,
long-term BM culture-initiating cells, and cobblestone-area-forming cells are CXCR4 dependent and essential for homing and engraftment of
nonobese diabetic (NOD)/severe combined immunodeficiency (SCID) mice
engrafting cells.13,18
On the basis of these results, we hypothesized that elevation of SDF1
in the peripheral circulation may result in significant mobilization of
HSCs and progenitor cells. In this regard, to explore the potential of
SDF1 to induce mobilization of hematopoietic cells, adenoviral (Ad)
vector expressing SDF1 (AdSDF1) was injected intravenously (IV) into
mice. Ad vectors are ideal vectors to deliver factors with chemokinetic
potential, such as SDF1, because they allow for sufficient plasma
elevation of a given chemokine for durations long enough to exert their
physiologic effect. The IV injection of Ad vectors expressing a given
chemokine results primarily in the localization of the Ad vectors to
the liver of mice facilitating constitutive release of chemokine
to the peripheral circulation.19 Duration of chemokine
expression is dependent on the rate of clearance of the Ad vector by
the immune response. Indeed, we have shown that IV injection of Ad
vector expressing thrombopoietin results in thrombocytosis for 10 days
in immunocompetent BALB/c mice, and it can last as long as 30 days
in immunodeficient SCID mice without any apparent
toxicities.20
In this report we demonstrate that IV injection of AdSDF1 into mice
resulted in profound mobilization of progenitors and cells with
repopulating capacity. In addition, AdSDF1 induced a remarkable increase in white blood cell (WBC) and platelet counts without any
apparent toxicity. On the basis of these results, we conclude that SDF1
may provide a useful means of mobilizing hematopoietic stem,
progenitor, and precursor cells.
Animals
Ad vectors
Immunoassays of SDF1 Human SDF1 in plasma and BM samples of Ad-treated mice were quantitated by SDF1 time-resolved fluoro-immuno assay (TRFIA)22 by using 2 anti-SDF1 antibodies (established by K.T. et al; Kyoto University, Kyoto, Japan). Each level of SDF1 shows the total of the levels of human SDF1 and human SDF1 . To obtain
murine BM samples for TRFIA, 5 mice in each group were humanely killed by cervical dislocation 3, 5, and 14 days after vector administration. BM was collected from these animals by aspiration of the BM from femur
and tibia.23
Peripheral blood analysis Initially, every 2 to 3 days and later on a weekly basis, retro-orbital blood was collected with capillary pipettes (Unopette; Fisher Scientific, Springfield, MA). Platelets, total WBCs, and granulocytes (polymorphonuclear leukocytes) were counted using a Neubauer hematocytometer (Fisher Scientific). Differential leukocyte counts were obtained by examination of blood smears from each mouse stained with Wright-Giemsa stain (200 cells counted/smear). The plasma was collected, stored at 80°C, and assessed later by immunoassay
for human SDF1.
Flow cytometry A total of 1 × 104 to 1 × 105 cells were incubated for 30 minutes at 4°C with fluorescein isothiocyanate (FITC)- or phycoerythrin (PE)-conjugated monoclonal antibodies (MoAbs); CD3-FITC (145-2C-11; Pharmingen, San Diego, CA), CD11b-FITC (M1/70; Pharmingen), Gr-1-PE (RB6-8C5; Pharmingen), Sca-1-PE (D7; Pharmingen), CD34-FITC (RAM34; Pharmingen), H-2Kb-FITC (AF6-88.5; Pharmingen), and H-2Kd-FITC (SF-1-1.1; Pharmingen). The cells were analyzed by 2-color flow cytometry using a Coulter Elite flow cytometer (Coulter, Hialeah, FL).Progenitor assay Three animals in each group were humanely killed 7 days following vector administration. One femur per animal was flushed with cold (4°C) Iscoves modified Dulbecco medium (IMDM)/20% fetal calf serum (FCS), and the total yield of BM and spleen mononuclear cells (MNCs) was determined by counting an aliquot in 0.36% acetic acid using a Neubauer hematocytometer. Peripheral blood MNCs (PBMNCs) were isolated after centrifugation over a discontinuous gradient using Lympholyte-M (Cederlane, Ontario, Canada). MNCs (105) were plated in triplicate in 1 mL 0.8% methylcellulose containing 30% FCS, 1% L-glutamine, 2.5% hemin, 0.05 mM 5-ME, recombinant mouse interleukin 3 (rm IL-3; 50 ng/mL; R&D Systems, Minneapolis, MN), rm c-kit ligand (20 ng/mL; Immunex, Seattle, WA), and recombinant human erythropoietin (2 U/mL; Sandoz, Basel, Switzerland) in 35-mm suspension culture dishes (Nunc, Naperville, IL). Cultures were incubated at 37°C in 100% humidity and 5% CO2 for 7 days. Scoring was performed with an inverted microscope with ×40 magnification on day 7.CFU-S assay For each data point, 3 recipient mice were irradiated with 9 Gy from a 137Cs -ray source at a dose rate of approximately
0.90 Gy per minute to prevent the production of endogenous spleen
colonies. Irradiated BALB/c mice (3 mice in each group) were injected
intravenously through the tail vein with 1 × 105 PBMNCs
within several hours after the completion of irradiation. The mice were
humanely killed by cervical dislocation 12 days later, and their
spleens were removed and fixed in Bouin solution. The number of
macroscopic spleen colonies was then scored.
Allogeneic peripheral blood cell transplantation After the vector administration, the peripheral blood from SCID mice (4 mice in each group) was collected on day 5 using Lympholyte-M (Cederlane) to remove erythrocytes. The recipient C57BL/6 mice (n = 8) were lethally irradiated (9.5 Gy) and intravenously injected with 1 × 106 PBMNCs of AdSDF1-treated SCID mice after irradiation on day 0. As a control, PBMNCs (1 × 106) of AdNull-treated SCID mice were transferred into irradiated C57BL/6 mice (n = 6). The chimeric mice were maintained in a laminar flow isolator. Chimerism was determined by flow-activated cell sorter (FACS) analyses (donor SCID mice, H-2Kd; recipient C57BL/6 mice, H-2Kb). The chimeric mice (at least 3) were humanely killed 90 days, 120 days, and 150 days after transplantation at each time point.Syngeneic peripheral blood cell transplantation After the vector administration, the peripheral blood from SCID mice (4 mice in each group) was collected on day 5 using Lympholyte-M (Cederlane) to remove erythrocytes. The recipient BALB/c mice (6 mice in each group) were lethally irradiated (9.5 Gy) and intravenously injected with serial cell doses (1 × 104, 1 × 105, and 1 × 106) PBMNCs after irradiation on day 0. Survival was monitored every day beyond day 150.Spleen and BM analyses BM was obtained by flushing both femoral bones with 3 mL cold IMDM containing 20% FCS. Manual leukocyte differentials were performed on Wright-Giemsa-stained cytospin preparations of BM cells and splenocytes.Histopathology Tissues were fixed in 10% buffered formalin and paraffin embedded. Sections were stained with hematoxylin and eosin and examined under microscopy.Statistical evaluation The results were expressed as mean ± SEM. Statistical analyses were performed using the unpaired 2-tailed Student t test. Survival rates were compared between the 2 groups by the log-rank test.
AdSDF1 promotes mobilization of leukocytes to the peripheral circulation Intravenous administration of AdSDF1 into SCID mice resulted in the elevation of SDF1 plasma levels, peaking at day 5 (2.5 ± 0.3 ng/mL) and returning to pretreatment level at day 35 (Figure 1A). However, IV administration of AdSDF1 resulted in only a small elevation of SDF1 levels (0.8 ± 0.1 ng/mL) in BM compared with plasma (*P < .005; Figure 1B). Plasma SDF1 was not detectable in the AdNull-treated mice.
To examine the effect of SDF1 in the peripheral blood in mobilization
of hematopoietic cells, we injected SCID mice intravenously with
109 pfu AdSDF1 on day 0 and monitored the change in
leukocyte number and hematopoietic progenitor frequency in BM, spleen,
and peripheral blood. As controls we used AdMIP3
AdSDF1 induces profound increase in platelet count We also monitored the change in platelet number in peripheral blood. Intravenous injection of AdSDF1 into SCID mice resulted in an increase in platelet count 3-fold above baseline 10 days after AdSDF1 administration (Figure 3A). Subsequently, platelets dropped to baseline levels by 6 weeks after injection. No significant increase in platelet levels was observed with administration of either AdMIP3 vector or AdNull (Figure
3B).
AdSDF1 promotes mobilization of progenitors (colony-forming
unit-culture [CFU-C]) and cells with the potential of CFU-S. AdSDF1 caused significant mobilization of CFU-C to the peripheral blood, predominantly colony-forming unit-granulocyte-macrophage (CFU-GM), as
compared to AdNull and normal control mice at day 5 (*P < .005), with the numbers of CFU-C returning to
control levels at day 10 (**P < .05; Figure
4A). CFU-Cs increased 15-fold in SCID
mice in peripheral circulation for 5 days.
The mobilization of progenitors was associated with a parallel decrease in progenitors within the BM. In fact, BM-derived CFU-C per femur significantly decreased in AdSDF1-treated SCID mice, compared with AdNull-treated SCID at day 7 (Figure 4B) (*P < .005). In contrast, in AdSDF1-treated mice, total numbers of CFU-C per spleen at day 7 were significantly increased when compared with AdNull-treated mice or age-matched normal mice. This was mainly due to an increase of CFU-GM (Figure 4B) (*P < .005). The formation of spleen colonies in the irradiated mice injected with SDF1-mobilized cells was also measured. Administration of AdSDF1 for 5 days caused a 24-fold increase in the peripheral blood cells of SCID mice CFU-S (day 12) (Figure 4C) (*P < .005). Administration of AdNull did not mobilize CFU-S (day 12) into the blood. Allogeneic peripheral blood cell transplantation Long-term reconstitutive ability was assessed using PBMNCs of adenovirus-treated SCID mice. After collecting the peripheral blood from SCID mice on day 5 after AdSDF1 and AdNull administration, PBMNCs (1 × 106) were transferred into lethally irradiated (9.5 Gy) C57BL/6 mice. After 150 days, H-2 typing showed that cells in the BM of chimeric mice that were transplanted with PBMNCs mobilized by AdSDF1 were more than 90% of donor H-2Kd-type origin (Figure 4D). In contrast, all chimeric mice died within 21 days after AdNull-treated PBMNC transplantation.Syngeneic peripheral blood cell transplantation Long-term reconstitutive ability was assessed using PBMNCs of AdNull- or AdSDF1-treated SCID mice (BALB/c background) in the syngeneic peripheral blood cell transplantation system. After collecting the peripheral blood from AdSDF1- and AdNull-treated SCID mice on day 5, different cell doses of PBMNCs (1 × 104, 1 × 105, and 1 × 106) were transferred into lethally irradiated (9 Gy) BALB/c mice. All mice were injected with various numbers of PBMNCs from AdNull-treated mice. Mice injected with 1 × 104 PBMNCs of AdSDF1-treated mice died within 17 days (Figure 4E). Two mice injected with 1 × 105 PBMNCs from AdSDF1-treated mice survived beyond 150 days. All of the mice transplanted with 1 × 106 PBMNCs from AdSDF1-treated mice survived beyond 150 days.Effect of AdSDF1 on spleen and BM The BM cellularity in AdSDF1-treated SCID mice was lower than AdNull-treated mice (Figure 5A) (**P < .05). Splenic cellularity increased at day 7 in the AdSDF1-treated SCID mice compared to AdNull-treated mice (Figure 5B) (*P < .005). The percentage of monocytes in the splenocytes of AdSDF1-treated mice was increased at day 7 compared to AdNull-treated mice. Histologically, there were regional decreases in cellularity in the BM of AdSDF1-treated mice at day 7 (Figure 6). However, at day 60, BM cellularity was normalized in AdSDF1-treated mice (not shown).
Among the known chemokines, SDF1 has been shown to induce chemotaxis of hematopoietic stem and progenitor cells in vitro.16-18,23 SDF1 is produced primarily by the BM stromal cells and seems to play a critical role in facilitating homing of HSCs and progenitors from fetal liver to the BM and establishing hematopoiesis. SDF1 also seems to be a key factor in maintaining HSCs in the BM during postnatal hematopoiesis. Therefore, we hypothesized that the SDF1-induced chemokinesis in conjunction with elevation in the extravascular space would result in mobilization of HSCs to the peripheral circulation. In this report, we demonstrate that elevation of SDF1 levels in the peripheral circulation results in mobilization of progenitors and cells with repopulating potential (CFU-S) into the peripheral circulation. SDF1 also induces an increase in platelets and WBCs. These data underscore the significance of SDF-1 in maintaining hematopoietic progenitors and precursors within the BM. Furthermore, these results suggest a role for SDF1 as an effective mobilization agent. Moreover, the time course of cell mobilization and changes in cell number paralleled SDF1 plasma levels suggest that SDF1-induced cell mobilization is controlled by a chemokine concentration gradient. Trafficking of HSCs is mediated through a combination of adhesion molecules and chemokines.24,25 At the present time the exact mechanism whereby HSCs home to the BM is not known. Studies have shown that interaction of HSCs with E-selectin and vascular cell adhesion molecule-1 seems to play a critical role in selective homing to the BM.26-28 Chemokines such as SDF1 orchestrate this process by providing directional cues for the HSCs to lodge within the BM microenvironment. Emerging data strongly suggest that CXCR4, the natural ligand for SDF1, is also expressed on HSCs as well as on mature monocytes, lymphocytes, neutrophils, megakaryocytes, and hematopoietic progenitors. Therefore, given the relatively large amounts of SDF1 released by the BM microenvironment, it is believed SDF1 plays a role in maintaining these cells within the marrow. According to studies, cytokines involved in stem cell mobilization, like SCF and IL-6, can up-regulate CXCR4 expression on CD34+ cells.29 Overnight incubation of CD34+ cells on a plastic surface could significantly increase the expression of CXCR4 at the cell surface. SDF1 itself increased colony formation by peripheral blood CD34+ cells in synergy with different cytokines.30 These data suggested that the SDF1/CXCR4 signal may play an important role in the stem cell engraftment and homing process, which involves not only chemokine and cytokine-induced mobilization and migration but also adhesion and proliferation of stem and progenitor cells. By using adenoviral vectors, we were able to increase the circulating
levels of SDF1 to 2.5 ng/mL. This level was sufficient to reverse the
gradient across the BM barrier, forcing CXCR4-expressing cells to exit
the BM. As a control chemokine, we overexpressed MIP3 We demonstrated that AdSDF1 induced migration of significant numbers of CFU-S. Among the known chemokines only IL-8 has been shown to effectively induce mobilization of CFU-S.31 In addition, injection of a limiting number of mobilized PBMNCs secondary to AdSDF1, but not AdNull, resulted in reconstitution of hematopoiesis in the recipient mice. Injection of as low as 1 × 105 PBMNCs mobilized by AdSDF1 resulted in reconstitution of hematopoiesis, strongly suggesting that subsets of SDF1-mobilized cells have stem cell potential. Therefore, given that mobilization of HSCs with repopulating capacity is critical for adequate peripheral stem cell collection and BM transplantation, SDF1 may provide a useful chemokine that could be incorporated into mobilization regimens. AdSDF1 induced a significant increase in the number of WBCs, including monocytes, neutrophils (Figure 2A,C), and immature myelomonocytic cells in both BALB/c and SCID mice. CXCR4 has been shown that it is expressed by all of these myeloid cells, suggesting that the primary mechanism resulting in their mobilization is mediated through SDF1. The increase in the platelet count was detected at day 5 after injection of the AdSDF1. We and other researchers have shown that CXCR4 is expressed on the mature polyploid megakaryocytes and platelets.32-34 SDF1 induces transendothelial migration of megakaryocytes and enhances platelet formations, possibly in extramedullary sites such as lung or spleen. Therefore, overexpression of SDF1 may also enhance migration of megakaryocytes and augment platelet release. In our studies presented here we needed to use adenoviral vectors to overexpress SDF1 to induce mobilization of progenitor cells. In fact, a single injection of recombinant SDF1 was ineffective in mobilizing progenitors (data not shown). These data suggest that constitutive production of high titers of SDF1 is essential to generate the reverse gradient and is essential for mobilization of the hematopoietic progenitor and stem cells. The CXCR4 expression by platelets as well as endothelial cells produces a large sink for circulating SDF1, thus increasing the requirement for constitutive production of high titers of SDF1 to induce elevated plasma levels. On the basis of the data presented, systemic overexpression of SDF1 provides a novel mechanism to induce multilineage mobilization of hematopoietic progenitor and precursor cells, mature monocytes, and platelets. This effect may not only be used clinically to recover HSCs for peripheral stem cell transplantation but also to improve clinical disorders in which there is profound multilineage pancytopenia. The use of Ad vectors to elevate the plasma levels of chemokine provides an efficient mechanism to induce transient increase in circulating progenitor and repopulating cells. These studies lay the foundation for examining the potential of SDF1 for mobilization of hematopoietic stem cells for gene therapy and cell transplantation.
We thank Harry G. Satterwhite, Maureen Sullivan, and Koji Shido for helpful assistance, Kate deBeer for preparing the manuscript, and Dr Masaya Ikegawa and Dr Kazuko Matsumoto for performing TRFIA studies. K.H. is the recipient of a fellowship from the Uehara Memorial Foundation (Tokyo, Japan). B.H. is the recipient of a fellowship from the Dr. Mildred Scheel Stiftung für Krebsforschung (Bonn, Germany).
Submitted September 26, 2000; accepted February 7, 2001.
Supported by National Institutes of Health (NIH) grant R01 HL-61401 (M.A.S.M.); the Gar Reichman fund of Cancer Research Institute. (M.A.S.M.); National Heart, Lung and Blood Institute (NHLBl) grants R01 HL-58707 (S.R.), R01 HL-61849 (S.R.); Program Project HL-66952 (Project 2) (S.R.); Pilot Project P01 HL-59312 (S.R.); the Dorothy Rodbell Foundation for Sarcoma Research (S.R.); the Rich Foundation (S.R.); R01 HL-57318 U01 (R.G.C.), U01 HL-66952-01 (R.G.C.); the Will Rogers Memorial Fund (R.G.C.); and GenVec, Gaithersburg, MD (R.G.C.).
The publication costs of this article were defrayed in part by page charge payment. Therefore, and solely to indicate this fact, this article is hereby marked "advertisement" in accordance with 18 U.S.C. section 1734.
Reprints: Malcolm A. S. Moore, James Ewing Laboratory of Developmental Hematopoiesis, Sloan-Kettering Institute for Cancer Research, 1275 York Ave, Mailbox 101, Rm 717, RRL, New York, NY 10021-6007; e-mail: m-moore{at}ski.mskcc.org.
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E. A. Sweeney, H. Lortat-Jacob, G. V. Priestley, B. Nakamoto, and T. Papayannopoulou Sulfated polysaccharides increase plasma levels of SDF-1 in monkeys and mice: involvement in mobilization of stem/progenitor cells Blood, January 1, 2002; 99(1): 44 - 51. [Abstract] [Full Text] [PDF]
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Top
Abstract
Introduction
E3
) or
AdNull-treated mice (
). All data are expressed as the mean
(n = 4) ± SEM. (B) In SCID mice, the concentration of human
SDF1 was measured in the plasma (
) and BM (
) of AdSDF1-treated
mice 3 days and 5 days after vector administration. All data are
expressed as the mean (n = 5) ± SEM. The result from SDF1 level
of BM compared to level of plasma achieves statistical significance
(*P < .005).
), and CFU-GEMM (
,
1 × 105 PBMNCs from ADSDF1-treated mice; 
,
1 × 104 PBMNCs from AdSDF1-treated mice; 
