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Topical Reviews |
1 Departments of Obstetrics and Gynecology, Perinatal Research Laboratories
2 Pediatrics
3 Animal Sciences, University of Wisconsin, Madison, WI 53715, USA
4 Department of Reproductive Medicine, Division of Maternal-Fetal Medicine, University of California, San Diego, CA 92093, USA
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Abstract |
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 Top Abstract IntroductionReferences |
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(Received 30 December 2004;
accepted after revision 17 March 2005;
first published online 24 March 2005)
Corresponding author J. Zheng: Departments of Obstetrics and Gynecology, Perinatal Research Laboratories, University of Wisconsin, 7E Meriter Hospital, 202 S Park Street, Madison, WI 53715, USA. Email: jzheng{at}wisc.edu
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Introduction |
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TopAbstractIntroductionReferences |
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Ang II is a well-characterized vasoconstrictor in systemic and uterine blood vessels. Of specific interest, however, is that during normal human and ovine pregnancies, high levels of the vasoconstrictor Ang II in both maternal and fetal circulations are temporally associated with dramatically increased placental blood flows (Iwamoto & Rudolph, 1981; Rosenfeld et al. 1993, 1995; Magness et al. 1994). For example, in pregnant women the circulating levels of Ang II are increased progressively (Robertson et al. 1971; Weir, 1975) during normal pregnancy and are elevated approximately 2.7-fold at late pregnancy as compared with those in non-pregnant women (Magness et al. 1994). More impressively, fetal Ang II production is even higher than the maternal production in both human (Broughton Pipkin et al. 1976; Oparil et al. 1978) and ovine (Naden et al. 1985; Mackanjee et al. 1991; Rosenfeld et al. 1995) pregnancies. This specific phenomenon is coupled to the refractoriness of placental vasculature to decreases in blood flow in response to infused Ang II. Moreover, coincident with the high levels of Ang II, fetoplacental vascular density increases 2- and 18-fold for the overall fetal placental and cotyledon, respectively (Reynolds & Redmer, 1995). Thus, the net result of these changes in the placenta vascular density, together with refractoriness of placental vasculature to Ang II and remodelling of the placenta vasculature (i.e. increase in its physical size; Annibale et al. 1990; Cipolla & Osol, 1994) is a marked reduction in placental vascular resistance and a dramatic increase in placental blood flow in spite of the rise in the levels of this potent vasoconstrictor Ang II.
Vascular contraction could be attenuated by secretion of vasorelaxing factors such as NO and prostacyclin (PGI2) from the endothelial cells. It is now increasingly apparent that the secretion of these endothelium-derived vasorelaxing factors is often under the direct control of many hormones classically associated with vascular smooth muscle (VSM) contraction, including Ang II, and that pregnancy in particular appears to selectively augment this endothelial response (Magness, 1993; Weiner et al. 1995). In pregnant sheep and pregnant women, the uterine artery demonstrates both increased NO and PGI2 production and attenuated increases in uterine vascular resistance in response to infused Ang II (McLaughlin et al. 1978; Everett et al. 1978; Magness et al. 1985, 1992). In sheep, the endothelium appears to be the sole source of this Ang II-induced increase in uterine artery PGI2 production because removal of the endothelium abolishes this response (Magness & Rosenfeld, 1993; Magness et al. 1996). Moreover, these responses in sheep appear unique to pregnancy because PGI2 production with Ang II treatment is not observed in the uterine artery in the non-pregnant state (Magness et al. 1985; Magness & Rosenfeld, 1993) and is unique to the uterine artery because Ang II does not increase PGI2 production from omental (systemic) artery segments from either non-pregnant or pregnant ewes (Magness et al. 1985, 1996). However, in other species such as dog, Ang II treatment can increase PGI2 release in various systemic vessels (i.e. renal and femoral arteries) (Shebuski & Aiken, 1980; Satoh et al. 1984).
Little is known about the roles of Ang II in regulating vasodilator production in the fetoplacental vasculature. It has been shown that Ang II is able to increase PGI2 production by the ovine fetoplacental artery (Yoshimura et al. 1990, 1991). However, PGI2 appears to fail to dilate fetoplacental vessels in vivo, even though it can reverse vasoconstriction induced by Ang II in fetal systemic blood vessels (Rankin et al. 1979; Parisi & Walsh, 1989) and attenuate the Ang II vasoconstrictive effect on human fetoplacental blood vessels in vitro (Tulenko, 1981; Mak et al. 1984; Glance et al. 1986). On the other hand, inhibition of NO-mediated guanylate cyclase activation increases the perfusion pressure of the human fetoplacental circulation (Myatt et al. 1991). In addition, inhibition of NOS activity with analogues of arginine potentiates vasoconstriction of human stem villous fetoplacental arteries (McCarthy et al. 1994) and increases ovine umbilical vascular resistance, leading to reduction in umbilical blood flow (Chang et al. 1992). These observations indicate that NO, a potent vasodilator, plays a pivotal role in regulating fetoplacental vascular tone during pregnancy (Sladek et al. 1997). However, whether Ang II can also enhance eNOS expression and NO production in the fetoplacental vasculature remains poorly understood.
Expression of Ang II receptors, eNOS and inducible NOS (iNOS) in fetoplacental vasculature
Although Ang II receptors are expressed in the placenta of many species, including human, bovine, porcine and ovine (Kalenga et al. 1991; Knock et al. 1994; Nielsen et al. 1996; Zheng et al. 1997; Li et al. 1998; Schauser et al. 1998; Cooper et al. 1999), the distribution of Ang II receptor subtypes in the placentas may differ among species and during different stages of pregnancy. For example, human fetal placental compartments and human placental villous blood vessels contain almost exclusively AT1-R (Kalenga et al. 1991; Knock et al. 1994; Li et al. 1998; Cooper et al. 1999). On the other hand, in bovine and porcine fetal placental compartments AT2-R appears to be predominant throughout pregnancy (Nielsen et al. 1996; Schauser et al. 1998). The ovine placenta expresses both AT1-R and AT2-R throughout pregnancy with a peak of expression occurring on day 45 of pregnancy (Koukoulas et al. 2002). Unlike bovine and porcine placentas, however, the ovine placenta expresses predominantly AT1-R at both mRNA and protein levels in early pregnancy (day 45), whereas levels of AT1-R and AT2-R expression are similar in late pregnancy (day 130) (Koukoulas et al. 2002). We have also localized AT1-R expression in ovine fetoplacental arteries (2nd or 3rd branches of the umbilical artery) (Zheng et al. 1998) and in ovine placentas (Zheng et al. 1997) from late pregnant ewes using immunohistochemistry (Fig. 1). In the fetoplacental arteries, AT1-R is present predominantly in the endothelium, with only a few cells stained in the underlying smooth muscle layer. These observations strongly suggest that Ang II may primarily act on fetoplacental artery endothelial cells rather than vascular smooth cells during late ovine pregnancy. We also found that during late ovine pregnancy, AT1-R is present in endothelial and smooth muscle cells of many microvessels (i.e. arterioles, venules and capillaries) in the fetal placental compartment, the cotyledon (COT; Fig. 1). AT1-R is also expressed in the majority of muscle cells in ovine myometrium (Zheng et al. 1997). This finding is in accordance with the report that AT1-R predominates (AT1-R : AT2-R 
80% : 20%) in myometrium during late ovine pregnancy although total Ang II binding decreases 
90% as compared with that in non-pregnant ewes where AT2-R is predominant (AT1-R : AT2-R 15% : 85%) (Cox et al. 1993). Similar phenomena are also observed in human myometrium, which contains almost entirely AT2-R (AT1-R : AT2-R 1% : 99%) during non-pregnancy, whereas during pregnancy AT1-R becomes predominant (AT1-R : AT2-R 66% : 34%) (de Gasparo et al. 1994; Bing et al. 1996). This alteration in distribution of Ang II subtype receptors in human myometrium appears to be due to down-regulation of AT2-R expression with no changes in AT1-R density (de Gasparo et al. 1994; Bing et al. 1996).
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Expression of AT1-R, AT2-R and eNOS in ovine fetoplacental artery endothelial cells
To investigate cellular and molecular mechanisms underlying the regulation of fetoplacental vascular functions, we have established a pure population of ovine fetoplacental artery endothelial (OFPAE) cells from a late pregnant ewe (Zheng et al. 1998). These cells were initially characterized using the uptake of acetylated low density lipoprotein and the expression of factor VIII, two classic markers for endothelial cells (Zheng et al. 1998). These OFPAE cells, even after prolonged culture in vitro (at least up to passage 18), still express AT1-R and eNOS, as observed in the fetoplacental arteries ex vitro (Fig. 1). The Ang II binding displacement experiments further demonstrate that both AT1-R and AT2-R are expressed in OFPAE cells with AT1-R as a predominant Ang II receptor subtype (75% of total Ang II binding sites) (Fig. 3, Zheng et al. 1999b). Expression of AT1-R and AT2-R is also found in human umbilical artery endothelial cells in culture (Zhang et al. 1999), although AT1-R is predominant in human fetal placental compartments and human placental villous blood vessels (Kalenga et al. 1991; Knock et al. 1994; Li et al. 1998; Cooper et al. 1999). These OFPAE cells also express several major receptors for bFGF and vascular endothelial growth factor (VEGF), and respond to bFGF and VEGF in a variety of bioassays such as cell proliferation and migration (Itoh et al. 1999; Zheng et al. 1999a; Tsoi et al. 2002; GenBank Accession no. AF534636). Thus, these cells in vitro maintain many in vivo characteristics and are an excellent cell model for studying fetal placental endothelial functions.
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Although it is generally accepted that Ang II is able to induce in vivo angiogenesis, as shown in both the chick chorioallantoic membrane and rabbit cornea assays (Fernandez et al. 1985; Le Nobel et al. 1991, 1993), the involvement of Ang II subtype receptors in this process is poorly defined. Recent evidence using several in vivo angiogenesis assays (i.e. the mouse matrigel and mouse ischaemic hindlimb model) has suggested that AT1-R in vivo positively modulates Ang II-stimulated angiogenesis, whereas AT2-R has no effect or plays a negative role (Munzenmaier & Greene, 1996; Silvestre et al. 2002; Tamarat et al. 2002a,b). However, opposite conclusions have also been made using the mouse alginate implant angiogenesis model by Walther et al. (2003), who demonstrated that AT2-R is angiogenic and AT1-R is anti-angiogenic after stimulation with endogenous Ang II. The causes of these discrepancies are unknown but are believed to be due to the different angiogenesis models used (Walther et al. 2003).
The critical role of AT1-R in mediating Ang II-induced endothelial cell proliferation and angiogenesis has also been recognized in other non-placental-derived endothelial cells in vitro. For instance, Monton et al. (1998) have reported that the AT1-R is largely responsible for Ang II-induced bovine aortic endothelial cell proliferation. On the other hand, AT2-R appears to play a negative role in Ang II-induced endothelial cell proliferation. This is supported by the studies of Stoll et al. (1995) who indicate that Ang II alone has no mitogenic effect on rat coronary artery endothelial cells expressing both AT1-R and AT2-R, but only blockade of AT2-R allows Ang II to stimulate cell proliferation via AT1-R activation. In OFPAE cells, Ang II dose-dependently stimulates cell proliferation with a biphasic pattern, being stimulatory at the relatively lower concentrations ranging from 0.01 to 10 nM and with no significant effect at a relatively high concentration (100 nM) (Fig. 4; Zheng et al. 1999b). Of particular interest is that the AT1-R antagonist DuP 753, but not the AT2-R antagonist PD 123319 at relatively low doses (0.1 and 1 µM), is sufficient to block Ang II-stimulated cell proliferation, while PD 123319 inhibits cell proliferation only at relatively high doses (10 and 100 µM). We believe that the inhibitory effects of PD 123319 are probably due to its non-specific cross-binding to AT1-R at these higher doses. Thus, it is likely that of two major Ang II subtype receptors, AT1-R is the primary mediator of Ang II-stimulated proliferation, and the low levels of AT2-R expression do not have a significant role in this stimulatory effect in OFPAE cells in culture. With AT1-R predominantly expressed in OFPAE cells (Fig. 3) and in human placental vasculature (Kalenga et al. 1991; Li et al. 1998; Cooper et al. 1999), it is likely that AT1-R is a key mediator for regulating Ang II-induced fetoplacental angiogenesis during ovine and human pregancies.
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Another potential intracellular signal for Ang II-induced placental angiogenesis could be NO since NO has been shown to lie downstream from Ang II-induced angiogenesis (Tamarat et al. 2002b). In OFPAE cells, we have recently also observed that Ang II elevates the production of NO (Fig. 6), which in turn could potentially activate ERK1/2, leading to OFPAE cell proliferation (J. Zheng, Y. X. Wen, J. L. Austin, D. B. Chen, unpublished observations). Beside NO, Ang II is also able to stimulate the production of superoxide anions in endothelial cells, possibly via AT1-R-mediated activation of membrane-bound NAD(P)H oxidases (Zhang et al. 1999; Gragasin et al. 2003), and production of peroxynitrite, which is formed by the reaction of NO and superoxide (Pueyo et al. 1998). Whether superoxide and peroxynitrite generated in response to Ang II will modulate Ang II-induced placental endothelial functions is unknown. However, it is generally believed that under normal physiological conditions superoxide and other reactive oxygen species are produced at low concentrations controlled tightly by a balance between pro-oxidant production and anti-oxidant capacity. Moreover, it has been reported that endothelial cells in culture appear to be more tolerant to the apoptotic effect of peroxynitrite than other cells (Lin et al. 1995). Thus, it is unlikely that superoxide and/or its derivatives will have significant negative effects on fetoplacental vascular growth and development under normal physiological conditions.
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Ang II regulation of vasodilatation via endothelial cell NO has been extensively studied although the exact mechanisms, particularly the involvement of Ang II subtype receptors, are not well understood (Henrion et al. 2001). It is believed that two Ang II subtype receptors may differentially mediate NO production depending on the size of vessels and the organ origins of vessels (Henrion et al. 2001). Moreover, Ang II may regulate NO-mediated vasodilatation through a paracrine mechanism (Tsutsumi et al. 1999). In this theory, it is postulated that overexpressed AT2-R in vascular smooth muscle cells induces bradykinin production, which in turn acts on adjacent endothelial cells and stimulates NO production, leading to vasodilatation (Tsutsumi et al. 1999). We have recently reported that Ang II dose- and time-dependently increases eNOS protein expression in OFPAE cells (Fig. 6; Zheng et al. 2005). Corresponding to this stimulatory effect, Ang II also increases total NO (nitrate and nitrite) production by OFPAE cells (Fig. 6). These data indicate that, similar to the uteroplacental vasculature (Magness et al. 1985, 1996), the high levels of Ang II in the fetal circulation during late pregnancy (Rosenfeld et al. 1993, 1995) may be capable of directly up-regulating local endothelial eNOS protein expression and endothelial NO production, so attenuating Ang II vasoconstriction action on the fetoplacental vascular smooth muscle. Our findings are in agreement with previous studies by other investigators using several non-placental-derived endothelial cells including bovine and porcine pulmonary arteries, rat aortic arteries, and human and bovine coronary microvasculature (Saito et al. 1996; Patel et al. 1999; Hill-Kapturczak et al. 1999; Bayraktutan, 2003; Gragasin et al. 2003; Olson et al. 2004; Batenburg et al. 2004).
Signalling mechanisms underlying Ang II-increased eNOS protein expression and NO production in OFPAE cells
The cellular effects of Ang II requires the rapid activation of receptor-linked, highly complex, intracellular signalling pathways including ERK1/2, p38 MAPK and protein kinase C (Griendling et al. 1997; Eguchi & Inagami, 2000). Whether these or other signalling pathways mediate the Ang II-regulated eNOS expression and endothelial NO production in OFPAE cells is unclear. Recently, we have assessed the role of the MEK–ERK1/2 cascade in Ang II-regulated eNOS expression and endothelial NO production in OFPAE cells (Zheng et al. 2005). By using several approaches, including immunocytochemistry, Western blot and immunocomplex kinase assays, Ang II activation of MEK–ERK1/2 in OFPAE cells is determined (Fig. 5, Zheng et al. 2005). PD 98059, a highly selective MEK inhibitor, almost completely inhibited the Ang II-increased eNOS protein levels, and partially, but significantly attenuated (31% reduction) the Ang II-elevated NO production (Fig. 6). Thus, these data indicate that the MEK–ERK1/2 cascade differentially modulates Ang II-increased eNOS protein expression and NO production in OFPAE cells. The activation of the MEK–ERK1/2 cascade is required and sufficient for Ang II-promoted eNOS protein expression. On the other hand, the activation of the MEK–ERK1/2 cascade is not sufficient for Ang II-elevated NO production, suggesting that additional distinct signalling events may be involved in elevating NO production. Such a premise is consistent with a growing body of evidence from studies of vascular smooth muscle cells showing that Ang II is capable of activating multiple signalling pathways, including ERK1/2, protein kinase C, and Jak/STAT (Griendling et al. 1997; Eguchi & Inagami, 2000). This phenomenon of differential regulation of eNOS protein expression and NO production is not surprising because the regulation of endothelial NO production could be through mediating eNOS protein levels and/or increasing eNOS enzymatic activity via acute phosphorylation or dephosphorylation of eNOS (Fulton et al. 2001; Fleming & Busse, 2003). Thus, NO production may not always be correlated with changes in eNOS protein expression.
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In conclusion, recent data from our laboratories suggest that Ang II is able to stimulate cell OFPAE cell proliferation primarily via AT1-R. Moreover, Ang II also increases eNOS protein expression and NO production at least partly via activation of the MEK–ERK1/2 cascade in OFPAE cells. Thus, these studies support our hypothesis that Ang II can stimulate fetoplacental angiogenesis, and increase endothelial NO production, which in turn may partly attenuate Ang II-induced vasoconstrictive action on vascular smooth muscle cells. Together, these Ang II-induced endothelial changes may lower overall fetoplacental vascular resistance, so modulating placental blood flow to support the rapidly growing fetus.
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