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Blood, Vol. 93 No. 10 (May 15), 1999:
pp. 3379-3390
Growth Factors and Cytokines Upregulate Gelatinase Expression in
Bone Marrow CD34+ Cells and Their Transmigration
Through Reconstituted Basement Membrane
Anna Janowska-Wieczorek,
Leah A. Marquez,
Jean-Marc Nabholtz,
Maria L. Cabuhat,
Jencet Montaño,
Hung Chang,
Jacob Rozmus,
James A. Russell,
Dylan R. Edwards, and
A. Robert Turner
From the Departments of Medicine and Oncology, University of Alberta,
Canadian Blood Services, Edmonton, Alberta, Canada; and the Departments
of Medicine and Biochemistry, The University of Calgary, Calgary,
Alberta, Canada.
The mechanism(s) underlying the release of stem/progenitor cells
from bone marrow into the circulation is poorly understood. We
hypothesized that matrix metalloproteinases (MMPs), especially gelatinases, which are believed to participate in the proteolysis of
basement membranes and in the migration of leukocytes, may facilitate
this process. First, we investigated whether CD34+
stem/progenitor cells express gelatinases A (MMP-2) and/or B (MMP-9)
and whether growth factors and cytokines (granulocyte colony-stimulating factor [G-CSF], granulocyte-macrophage
colony-stimulating factor [GM-CSF], stem cell factor [SCF],
macrophage colony-stimulating factor [M-CSF], interleukin-3 [IL-3],
IL-6, IL-8, and tumor necrosis factor- [TNF-]) are
able to modulate their expression. Next, we examined the transmigration
of these stem/progenitor cells through reconstituted basement membrane
(Matrigel) and its modulation by growth factors and cytokines.
CD34+ cells were obtained from steady-state bone marrow
and peripheral blood (from leukapheresis products collected either in
steady-state hematopoiesis or after mobilization with G-CSF plus
chemotherapy or G-CSF alone). We found that peripheral blood
CD34+ cells, regardless of whether they were mobilized or
not, strongly expressed both gelatinases (MMP-2 and MMP-9) in contrast
to steady-state bone marrow CD34+ cells, which did not.
However, all the growth factors and cytokines tested could induce MMP-2
and MMP-9 secretion by the latter cells. Moreover, the stimulatory
effects of G-CSF and SCF on both MMP-2 and MMP-9 secretion were found
to be significantly higher in CD34+ cells isolated from
bone marrow than in those from peripheral blood. In addition TNF-,
GM-CSF, and IL-6 increased the secretion of a partially active form of
MMP-2. Basal transmigration of bone marrow CD34+ cells
through Matrigel was lower than that of peripheral blood CD34+ cells (P < .0001), but growth factors and
cytokines increased it by 50% to 150%. Positive correlations were
established between expression of gelatinases and CD34+
cell migration (r > .9). The stimulatory effect of G-CSF was significantly greater on the migration of CD34+ cells
from bone marrow than on those from peripheral blood (P = .004). Moreover, CD34+ cell migration was reduced to
approximately 50% by antibodies to MMP-2 and MMP-9, tissue inhibitors
of metalloproteinases (rhTIMP-1 and -2), and
o-phenanthroline. TNF--induced gelatinase
secretion and migration of CD34+ cells and of clonogenic
progenitors (colony-forming unit-granulocyte-macrophage [CFU-GM], burst-forming unit-erythroid [BFU-E],
colony-forming unit granulocyte, erythroid, monocyte,
megakaryocyte [CFU-GEMM], and colony-forming
unit-megakaryocyte [CFU-MK]) were dose-dependent. Therefore, this study demonstrated that CD34+ cells that
are circulating in peripheral blood express both MMP-2 and MMP-9 and
transmigrate through Matrigel. In contrast, CD34+ cells
from steady-state bone marrow acquire similar properties after exposure
to growth factors and cytokines, which upregulate expression of
gelatinases and transmigration of these cells when they enter the
bloodstream. Hence, we suggest that growth factors and cytokines induce
release of stem/progenitor cells from bone marrow into peripheral blood
during mobilization, as well as during steady-state hematopoiesis, by
signaling through gelatinase pathways.
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