Brief Reviews |
From the Divisions of Cardiovascular Medicine and Research, St. Elizabeths Medical Center, Boston, Mass.
Correspondence to Douglas W. Losordo, MD, Divisions of Cardiovascular Medicine and Research, St. Elizabeths Medical Center, 736 Cambridge St, Boston, MA 02135. E-mail dlosordo{at}opal.tufts.edu
| Abstract |
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Key Words: estrogen angiogenesis vasculogenesis endothelium endothelial progenitor cells
| Introduction |
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knockout mouse, in which angiogenesis is
impaired,3 and by the
demonstration that estrogen receptor antagonists can
inhibit angiogenesis.4 The
positive correlation between estrogen receptor expression, angiogenic
activity, and breast tumor invasiveness also supports the angiogenic
effect of estrogen mediated by the estrogen
receptor(s).5 6 7 8
Finally, some reports suggest that the antitumor effect of tamoxifen
may in fact relate to an antiangiogenic action of this estrogen
receptor
agonist/antagonist.9 Several additional lines of experimental evidence suggest that estrogen and other sex steroids play important roles in physiological and pathological angiogenesis. One of the first observations suggesting a hormonal influence on angiogenesis was an inhibitory effect on tumor vascularization by medroxyprogesterone.10 Subsequent studies have indicated that the mechanism of this inhibition may relate to the regulation of thrombospondin-1, an angiogenesis inhibitor, by this hormone.11
Angiogenesis has been noted to be a prognostic marker in breast cancer,12 and inhibition of angiogenesis in these tumors has been effected by antiestrogens.4 In addition, the estrogen metabolite 2-methoxyestradiol has been shown to be a potent antiangiogenic agent13 mediated by actions on cytoskeletal structure14 and by increasing endothelial cell apoptosis.15 16
| Vascular Endothelial Cell Proliferation and Migration Are Enhanced by Estradiol |
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| Role of VEGF in Estrogen-Mediated Angiogenesis |
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| Role of NO in Estrogen-Mediated Angiogenesis |
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The role of NO in angiogenesis has been controversial. Previous reports have suggested that NO inhibits the migration of endothelial cells,39 which is an essential step in angiogenesis.40 In addition, NO donors have been shown to inhibit angiogenesis in vitro41 and in vivo.42 More recently, however, NO has been shown to be critical for the angiogenic properties of VEGF.43 Finally, and most compelling, the angiogenic response to ischemia has been shown to be severely impaired in a mouse model with targeted disruption of endothelial NO synthase,44 and these mice have also displayed delayed endothelial recovery after vascular injury.45
| Regulation of Adhesion Molecule Expression by Estrogen |
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| Vascular Cells Express Estrogen Receptors |
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has been
demonstrated in endothelial
cells18 19 and
vascular SMCs.53 54
In addition to the
form of the receptor, the ß isoform has also
been demonstrated in vascular tissue with increased expression after
vascular injury,55 although
the function of the ß-receptor in vascular tissue has not yet been
fully
defined.56 | Effect of Estrogen on Bone Marrow Precursors |
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,63 and an intact
estrogen receptor transactivation domain has been shown to be required
for estradiol to inhibit the differentiation of avian erythroid
progenitors.64 Interestingly,
estradiol has also been shown to regulate erythropoietin
production locally in the uterus in association with angiogenic
activity in that organ.65
Together, these prior studies provide evidence of direct actions of
estradiol on the bone marrow and the regulation of bone marrowderived
precursor cells. | Steroid HormoneMediated Recruitment of Inflammatory Cells to the Uterus |
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| Role of MPs in the Uterus |
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In addition, uterine epithelial cells and endometrial stromal cells are also the source of a number of cytokines, such as VEGF,22 23 which may influence angiogenesis by directly inducing endothelial cell proliferation83 or by recruiting endothelial progenitor cells.84
| Mechanisms of Angiogenesis |
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During angiogenesis, migration precedes proliferation by
24 hours.86 This principle
was best demonstrated in classic experiments performed by Sholley et
al,40 who used a model of
inflammation-induced angiogenesis of the rat cornea, in which
initiation of vascular sprouting was shown to occur in the absence of
endothelial cell proliferation, which was suppressed by
x-irradiation before application of the inflammatory stimulus. In
irradiated corneas displaying no cellular proliferation, vascular
sprouting at 2 days was similar to that seen in contralateral shielded
corneas. Although neovascular growth was subsequently blunted and
ultimately ceased by 4 to 7 days, these experiments documented the
critical if not exclusive roles of migration and redistribution of
preexisting endothelial cells in the commencement of
neovascularization. Similar implications resulted from work by Nicosia
et al87 : Fibronectin was
shown to promote, in a dose-dependent fashion, the elongation of
microvessels that sprout from explants of rat aorta placed in
serum-free collagen gel, despite the fact that neither DNA synthesis
nor mitotic activity was increased in serum-free collagen gels compared
with fibronectin-negative gels. Therefore, fibronectin was inferred to
promote angiogenesis in vitro by migratory recruitment of preexisting
endothelial cells. Subsequent studies have established
the critical role played by plasmin and other proteases in promoting
migration through preexisting
matrix.88 89
In contrast to angiogenesis in vivo inflammatory and in vitro organ culture models, angiogenesis that develops in response to experimental vascular obstruction, ie, collateral vessel development, has been shown by several previous investigators to involve proliferation of not only endothelial cells but also SMCs. Several important principles have been elucidated by these studies.
First, evidence of endothelial cell proliferation is nearly absent in normal arteries,90 91 a finding that is consistent with an estimated endothelial cell turnover time of "thousands of days" in quiescent microvasculature.92 Even a relatively low percentage of endothelial cell proliferation observed in response to arterial occlusion or exogenous growth factors may therefore represent considerable enhancement of endothelial cell proliferative activity and, when considered in relation to a denominator of thousands of endothelial cells, is clearly sufficient to provide the basis for new blood vessel formation. Second, endothelial cell proliferation that contributes to naturally occurring collateral development in the setting of vascular occlusion varies from 2.6% to 3.5% in the canine coronary90 93 and from 5% to 6% in the rodent renal vasculature94 and is <1% in swine coronary arteries.95 The contrasting rates of endothelial cell proliferation between the canine and swine coronary circulations are in parallel with the relative propensity for natural collateral artery development in these 2 species. Third, proliferation of SMCs, the additional requisite cell type for the formation of larger blood vessels, is an implicit component of angiogenesis, regardless of animal species or circulatory site.96 Fourth, proliferative activity (for SMCs as well as endothelial cells) is highest at the level of the smallest-diameter collateral vessels, the so-called midzone collateral segments.90 93 97 98 Fifth, although evidence of endothelial cell and SMC proliferation alone does not necessarily distinguish new vessel development from an increase in the size of preexisting vessels, adjunctive data regarding increased capillary density83 99 support the notion that proliferative activity does in fact reflect true angiogenesis.
| Postnatal Vasculogenesis |
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Postnatal neovascularization has been previously considered
to result exclusively from the proliferation, migration, and remodeling
of fully differentiated endothelial cells derived from
preexisting blood vessels, ie, angiogenesis (see
Figure
).90 92 100
The formation of blood vessels from EPCs (ie, vasculogenesis) has been
considered to be restricted to
embryogenesis.101 105
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However, we reasoned that the use of hematopoietic stem cells derived from peripheral blood in lieu of bone marrow to provide sustained hematopoietic recovery constituted inferential evidence for circulating stem cells. Circulating CD34 antigenpositive EPCs were recently isolated from adult species; once adherent, these cells were shown to differentiate along an endothelial cell lineage in vitro.106 Heterologous, homologous, or autologous EPCs administered systemically to animals with operatively induced hindlimb ischemia were found to incorporate themselves into foci of neovascularization in ischemic muscles of the affected hindlimb. These findings, together with those of other recent studies,107 108 109 110 have been interpreted as evidence of postnatal "vasculogenesis."101 105
| Hormone-Regulated Neovascularization |
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Despite clinical evidence of the significant role of steroid hormones in endometrial neovascularization, the results of previous experiments have yielded inconclusive results in terms of defining specific elements of pathophysiological mechanisms, including experiments involving endothelial cells in vitro and in vivo.3 4 10 17 119 120 121 Moreover, estrogen has been shown to exhibit an inhibitory effect on certain hematopoietic kinetics, including lymphocytes and monocytes, numerically60 122 123 and functionally.124 125
Conventionally, endometrial vascularization has been considered to develop as the result of angiogenesis, ie, proliferation and migration of fully differentiated endothelial cells (endothelial cells) from preexisting "parent" vessels.126 However, normal monthly physiological endometrial proliferation would require that endothelial cells in the uterus replicate >1000 times during the reproductive life span of the average human female. Therefore, it is unlikely that differentiated endothelial cells in situ could accomplish this mission without the occurrence of replicative senescence.127
As outlined above, a large body of previous literature has documented the recruitment of MPs and other nucleated cells to the uterus under the influence of sex steroids. Our data128 indicate that a subpopulation of these cells is capable of differentiating into endothelial cells (ie, EPCs) and thereby constitutes a previously unidentified source of vascular cells for cyclical neovascularization. In future studies, we will explore the influence of estradiol on EPC recruitment, differentiation, and incorporation in several models of postnatal angiogenesis/vasculogenesis.
| Conclusions |
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| Acknowledgments |
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Received April 3, 2000; accepted August 15, 2000.
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