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Next Article 
Blood, Vol. 92 No. 8 (October 15), 1998:
pp. 2609-2612
Adhesion Receptors as Regulators of the Hematopoietic Process
By
C.M. Verfaillie
From the Division of Hematology, Oncology and Transplantation,
Department of Medicine, University of Minnesota, Minneapolis, MN.
HEMATOPOIESIS IS A complex process in
which pluripotent stem cells proliferate and differentiate to generate
the full complement of mature blood cells. More than 30 hemopoietic
cytokines and growth factors that increase or decrease progenitor
proliferation and differentiation have been cloned and
characterized.1-3 Although the biological effects of these
cytokines and growth factors on stem and progenitor cells has been
extensively studied, we still do not understand how this extremely
orderly hematopoietic process is regulated. Under steady-state
conditions, hematopoiesis takes place within the bone marrow
microenvironment. Stem cells and their progeny interact relatively
specifically with cell and extracellular matrix (ECM) ligands present
in the marrow but not other microenvironments.4-6 These
adhesive interactions are responsible for the retention of
hematopoietic cells in the marrow. Like hematopoietic cells, hematopoietic cytokines and growth factors bind to some specific extracellular matrix components7,8 and stromal cells can express certain cytokines on their surface.9 Selective
adhesion of progenitors and cytokines to ECM components or stromal
cells then results in the colocalization of progenitors at a specific stage of differentiation with a specific array of cytokines, in so-termed niches.10,11 This provides one level of growth
and differentiation regulation. There is also mounting evidence that contact interactions per se between progenitors and marrow stromal ligands play an important role in the regulation of the hematopoietic process.12-14 Adhesive interactions themselves may serve as
growth or survival signals or adhesion itself may modulate cytokine- or
growth factor-dependent signals. These contact-mediated cues may be
responsible for regulating the orderly progression of hematopoiesis.
More than 20 different adhesion receptors have been identified on
hematopoietic progenitors.15,16 These include members of
the integrin family responsible for adhesion to ECM components (fibronectin, collagen, laminin, or thrombospondin)17 or
cell surface-expressed cell adhesion molecules (CAM; vascular [VCAM] and intracellular [ICAM]).18,19 Progenitors express
CD44,20 which supports adhesion to
hyaluronate20,21 and fibronectin.22 Platelet-endothelial-(PE) CAM-1, a member of the Ig superfamily of cell
adhesion molecules, and L-selectin are expressed on
progenitors.23,24 Finally, several sialomucins have been
found on progenitors, including the stem cell antigen,
CD34,25 CD43,26,27 CD45RA,28
P-selectin glycoprotein ligand-1 (PSGL-1),29 and CD164,
described by Zanettino et al30 in this issue of
BLOOD.31 Other members from this family not
expressed on hematopoietic cells include glycosylation-dependent
cell-adhesion molecule-1 (Glycam-1)32 and mucosal addressin
cell adhesion molecule-1 (Madcam-1).33
Which of these receptors is responsible for the specific retention of
stem and progenitor cells in the marrow microenvironment or the homing
of progenitors to the marrow is not known. In vitro, adhesion of
CD34+ cells to stromal feeders can be blocked by antibodies
against the majority of these receptors.17-24,30,31 In vivo
experiments have suggested a relatively predominant role of
 1-integrins in the retention of progenitors in the marrow and
progenitor homing to the marrow.34-36 However,
1-integrins and their ligands are ubiquitously expressed and
1-integrins cannot provide for the rather exclusive
progenitor-marrow interactions. Thus, another receptor(s) must be
responsible for the specific stem cell-marrow interactions. The mucin
receptor, CD164, described by Zanettino et al,30 or
similar as yet to be characterizedglycoprotein receptors may provide
such specificity. In contrast to integrins, whose structure is
identical on all cell types, a number of splice variants of CD164
exist, some of which are expressed on endothelial cells but not on
hematopoietic cells.30,31 Differences in the glycosylation
pattern of CD164 or like molecules may provide further specificity to
the receptor.37,38 It has long been speculated that homing
of stem cells to the marrow microenvironment depends on lectin-mediated
interactions.4 If the sialomucin, CD164, is such a homing
receptor, will need to be shown by in vivo transplantation of
progenitors from CD164 / animals.
Besides being responsible for anatomical localization, adhesion
receptors can also transmit signals that modulate the response of the
cell to other extracellular factors or directly induce or inhibit cell
proliferation, survival, and differentiation. In other biological
systems, outside-in signals through integrins and selectins have been
most extensively studied.39-42 Engagement of these
receptors activates a number of signaling pathways involved with cell
proliferation, survival, and differentiation. In the hematopoietic
system, coculture of progenitors with stromal feeders inhibits
proliferation of progenitors.12-14 The exact mechanism underlying this observation is still unknown. A number of studies have
shown that engagement of integrins,14,43-45
selectins,46 and, now, mucins31 has profound
effects on progenitor survival and growth and may account for the
observed contact mediated effects on progenitor proliferation,
differentiation, and survival. For instance, when integrins are engaged
on CD34+ cells cultured with pharmacological concentrations
of cytokines, significantly more quiescent progenitors are recruited in
cell cycle.44 In contrast, when CD34+ cells are
cultured under low, more physiological cytokine conditions, engagement
of integrins prevents progression of CD34+ cells from the
G1 to S phase of the cell cycle, therefore inhibiting progenitor proliferation.14,43 Finally, integrin engagement on CD34+ cells cultured in the absence of cytokines or
serum serves as a survival signal.45 These studies
illustrate that integrin-engagement can affect survival and growth of
hematopoietic progenitors. Second, these studies illustrate that
regulation of hematopoiesis may be the result of a combined effect of
cytokines and contact mediated interactions.
Integrins do not display an enzymatic activity that might serve to
trigger a cellular response.47 Signaling requires that the
cytoplasmic tail of the integrin colocalizes with the cellular cytoskeleton, which then recruits and activates a tyrosine kinase such
as focal adhesion kinase (Fak).48 This leads to activation of Ras, which affects cell proliferation; activation of
phosphoinositol-3 kinase (PI-3K), which affects cell proliferation and
survival; and alterations in the levels of cyclins, cyclin-dependent
kinases, and cyclin-dependent kinase
inhibitors.49-51 Which of these pathways are
involved in integrin-mediated regulation of hematopoietic progenitor
proliferation, differentiation, and survival is not yet clear.
In the accompanying report, Zanettino et al30 present
evidence that engagement of the mucin, CD164, on normal
CD34+ cells prevents recruitment of quiescent hematopoietic
progenitors into cell cycle when stimulated with a cocktail of
cytokines. Engagement of this receptor on
CD34+CD38 cells induces apoptotic cell death
in a large proportion of these cells. The effect of CD164 engagement
under different cytokine conditions has not been tested. Because the
natural ligand for CD164 is unknown, CD164 receptors were engaged with
adhesion blocking anti-CD164 antibodies, a method commonly used in
integrin-mediated signaling studies.
Another example of mucin-mediated signaling in hematopoietic cells is
prevention of terminal differentiation of myeloid cells seen after
enforced expression of CD34,52 an effect
dependent on the cytoplasmic tail of the molecule. Consistent with
these in vitro studies demonstrating a role for CD34 in prevention of terminal differentiation is the finding that the progenitor population in yolk sac as well as in marrow or spleen of CD34/
mice is significantly decreased,53 possibly as a result of premature terminal differentiation.
The signal pathways activated by mucin receptors are yet to be
identified. As for integrin receptors, the cytoplasmic tails of mucin
receptors do not have intrinsic kinase or other enzymatic function.
However, mucins may interact with the cell cytoskeleton through the
actin-binding proteins, ezrin and moesin.54 The effect of
mucin receptor engagement on intracellular signals has been studied in
a number of different cell types, but not yet in hematopoietic
progenitor and stem cells. Stimulation of mucin receptors may activate
protein tyrosine kinase, the phospholipase C/phosphoinositides
signaling pathways, and G-protein signal pathways.55-57 Which signal pathways cause cell death or inhibition of cell
proliferation or differentiation after stimulation of the CD164
receptor, or other sialomucin receptors, on hematopoietic cells still
needs to be determined.
The work describing the cloning and initial functional analysis of a
novel adhesion receptor expressed on hematopoietic progenitors illustrates the fact that the hematopoietic process, like other complex
biological systems, is governed not only by signals from classically
defined cytokines and growth factors, but also by other interactions
between the hematopoietic cell and its microenvironment. These
cell-cell and cell-ECM contact interactions are responsible not only
for the localization of hematopoietic progenitors in the marrow, but
also play an important role, like cytokine receptors, in the regulation
of progenitor proliferation. Future studies characterizing the signals
emanating from adhesion receptors on hematopoietic progenitors will
lead to a better insight in the mechanisms that govern the tightly
regulated process of normal hematopoietic cell proliferation and
differentiation. Such insights may then lead to improved methods for ex
vivo manipulation of hematopoietic stem and progenitor cells. There is
already evidence that aberrant adhesive interactions caused by
decreased function58 or expression59,60 of
certain adhesion receptors may underlie the premature mobilization of
progenitors in the peripheral blood in certain leukemias and that these
defects may in part cause the deregulated proliferation and
differentiation seen in leukemic transformation. Future efforts by
basic biologists and clinicians are needed to identify potential
abnormalities in contact-mediated regulation of progenitor
proliferation and differentiation in pathological conditions
characterized by increased (leukemias) or decreased (hypoplasia)
progenitor growth. This may lead to a better understanding of the
pathogenesis of these diseases and new therapeutic approaches for these
disorders.
 |
FOOTNOTES |
Address reprint requests to C.M. Verfaillie, MD, Department of
Medicine, University of Minnesota, Box 806 UMHC, 422 Delaware St SE,
Minneapolis, MN 55455; e-mail: verfa001{at}tc.umn.edu.
| |
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