Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-8448b6f56d-sxzjt Total loading time: 0 Render date: 2024-04-24T21:41:02.205Z Has data issue: false hasContentIssue false

5 - The renin–angiotensin system in pre-eclampsia

from Part I - Basic science

Published online by Cambridge University Press:  03 September 2009

By
Fiona Broughton Pipkin
Edited by
Fiona Lyall  and
Michael Belfort
Fiona Lyall
Affiliation:
University of Glasgow
Michael Belfort
Affiliation:
University of Utah
Get access

Summary

Angiotensin II (AngII) has suffered from being a hormone with a long history. Like an aging film star, it has tended to be overlooked. The renin–angiotensin system (RAS) was among the first hormone systems to be studied when Tigerstedt and Bergman described how intravenously injected saline extracts of kidney caused pronounced hypertension in rabbits (Tigerstedt and Bergman, 1898), and it is as a vasoconstrictor system that the RAS has largely been regarded ever since. This is, however, only one aspect of the chameleon-like RAS. AngII has autocrine and paracrine effects, as well as effects as a classic circulating hormone. Furthermore, fragments of angiotensin can have widely differing actions, and can work through receptors other than the well-described types 1 and 2. This chapter will consider the circulating RAS in pre-eclampsia as well as its effects as a paracrine system in relation to cell proliferation, differentiation and apoptosis, interaction with other cytokines, vascular media hypertrophy, endothelial dysfunction and atherothrombosis. Many of these have not yet been studied in relation to pre-eclampsia, but the parallels with non-pregnant hypertension suggest strongly that they should be.

Synthesis

The enzyme renin, an aspartyl protease, has only one substrate, the α2-globulin angiotensinogen (Aogen) (Poulsen and Jacobsen, 1993). The converse, however, is not true. Aogen acts as a substrate for a number of other enzymes, among them cathepsins D and G, tonin and tissue plasminogen activator (Dzau et al., 1988; Klickstein et al., 1982), all of which can cleave it, some apparently resulting in the direct synthesis of AngII without the intervening production of angiotensin I (AngI).

Type
Chapter
Information
Pre-eclampsia
Etiology and Clinical Practice
 , pp. 78 - 91
Publisher: Cambridge University Press
Print publication year: 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aalkjaer, C., Johannesen, P., Pedersen, E. B., Rasmussen, A. and Mulvany, M. J. (1984). Morphology and angiotensin II responsiveness of isolated resistance vessels from patients with pre-eclampsia. Scand. J. Clin. Lab. Invest., 169(Suppl.), 57–60.CrossRefGoogle ScholarPubMed
Ahmed, A., Li, X. F., Shams, M., et al. (1995). Localization of the angiotensin II and its receptor subtype expression in human endometrium and identification of a novel high-affinity angiotensin II binding site. J. Clin. Invest., 96, 848–57.CrossRefGoogle ScholarPubMed
Albiston, A. L., McDowall, S. G., Matsacos, D., et al. (2001). Evidence that the angiotensin IV (AT4) receptor is the enzyme insulin-regulated aminopeptidase. J. Biol. Chem., 276, 48,623–6.CrossRefGoogle ScholarPubMed
Allen, J., Forman, A., Maigaard, S., Jespersen, L. T. and Andersson, K. E. (1989). Effect of endogenous vasoconstrictors on maternal intramyometrial and fetal stem villous arteries in pre-eclampsia. J. Hypertens., 7, 529–36.CrossRefGoogle ScholarPubMed
Ardaillou, R. and Chansel, D. (1997). Synthesis and effects of active fragments of angiotensin II. Kidney Int., 52, 1458–68.CrossRefGoogle ScholarPubMed
Arngrimsson, R., Geirsson, R. T., Cooke, A., Connor, M., Bjornsson, S. and Walker, J. J. (1994). Renin gene restriction fragment length polymorphisms do not show linkage with preeclampsia and eclampsia. Acta Obstet. Gynecol. Scand., 73, 10–13.CrossRefGoogle Scholar
Baker, P. N., Broughton Pipkin, F. and Symonds, E. M. (1992). Longitudinal study of platelet angiotensin II binding in human pregnancy. Clin. Sci. (Lond.), 82, 377–81.CrossRefGoogle ScholarPubMed
Bashford, M. T., Hefler, L. A., Vertrees, T. W., Roa, B. B. and Gregg, A. R. (2001). Angiotensinogen and endothelial nitric oxide synthase gene polymorphisms among Hispanic patients with preeclampsia. Am. J. Obstet. and Gynecol., 184, 1345–50.CrossRefGoogle ScholarPubMed
Benndorf, R., Boge, R. H., Ergun, S., Steenpass, A. and Wieland, T. (2003). Angiotensin II type 2 receptor inhibits vascular endothelial growth factor-induced migration and in vitro tube formation of human endothelial cells. Circ. Res., 93, 438–47.CrossRefGoogle ScholarPubMed
Bing, C., Johnson, I. R. and Broughton Pipkin, F. (1996). Angiotensin receptors in myometrium and myometrial vessels from uteri of women during the follicular and luteal phases of the menstrual cycle and in late pregnancy. Clin. Sci. (Lond.), 90, 499–505.CrossRefGoogle ScholarPubMed
Broughton Pipkin, F. (1993). The renin system and reproduction in animals. In The Renin–Angiotensin System, vol. 1. ed. Robertson, J. I. S. N. and Nicholls, M. G.. London: Gower Medical Publishing. pp. 49.41–49.49.Google Scholar
Broughton Pipkin, F., Craven, D. J. and Symonds, E. M. (1981). The utero-placental renin–angiotensin system in normal and hypertensive pregnancy. Contrib. Nephrol., 25, 49–52.CrossRefGoogle Scholar
Broughton Pipkin, F., Sharif, J. and Lal, S. (1995). Angiotensin and asymmetric fetal growth. Lancet, 346, 844–5.CrossRefGoogle ScholarPubMed
Brown, J. J., Davies, D. L., Doak, P. B., Lever, A. F., Robertson, J. I. and Tree, M. (1964a). The presence of renin in human amniotic fluid. Lancet, ii, 64–6.CrossRefGoogle Scholar
Brown, J. J., Davies, D. L., Doak, P. B., Lever, A. F., Robertson, J. I. and Trust, P. (1964b). Plasma renin concentration in the hypertensive diseases of pregnancy. J. Obst. Gynaecol. Br. Commonwlth, 73, 410–17.CrossRefGoogle Scholar
Bussen, S. S., Sutterlin, M. W. and Steck, T. (1998). Plasma renin activity and aldosterone serum concentration are decreased in severe preeclampsia but not in the HELLP-syndrome. Acta Obstet. Gynecol. Scand., 77, 609–13.CrossRefGoogle Scholar
Campbell, D. C. and Kladis, A. (1990). Simultaneous radioimmunoassay of six angiotensin peptides in arterial and venous plasma of man. J. Hypertens., 8, 165–72.CrossRefGoogle Scholar
Celerier, J., Cruz, A., Lamande, N., Gasc, J. M. and Corvol, P. (2002). Angiotensinogen and its cleaved derivatives inhibit angiogenesis. Hypertension, 39, 224–8.CrossRefGoogle ScholarPubMed
Cesari, M., Rossi, G. P. and Pessina, A. C. (2002). Biological properties of the angiotensin peptides other than angiotensin II: implications for hypertension and cardiovascular diseases. J. Hypertens., 20, 793–9.CrossRefGoogle ScholarPubMed
Chapman, A. B., Abraham, W. T., Zamudio, S., et al. (1998). Temporal relationships between hormonal and hemodynamic changes in early human pregnancy. Kidney Int., 54, 2056–63.CrossRefGoogle ScholarPubMed
Cooper, A. C., Robinson, G., Vinson, G. P., Cheung, W. T. and Broughton Pipkin, F. (1999). The localization and expression of the renin–angiotensin system in the human placenta throughout pregnancy. Placenta, 20, 467–74.CrossRefGoogle ScholarPubMed
Craven, D. J., Warren, A. Y. and Symonds, E. M. (1983). Generation of angiotensin I by tissues of the human female genital tract. Am. J. Obstet. Gynecol., 145, 749–51.CrossRefGoogle ScholarPubMed
Curnow, K. M., Pham, T. and August, P. (2000). The L10F mutation of angiotensinogen is rare in pre-eclampsia. J. Hypertens., 18, 173–8.CrossRefGoogle ScholarPubMed
Gasparo, M. (2002). Angiotensin II and nitric oxide interaction. Heart Fail. Rev., 7, 347–58.CrossRefGoogle ScholarPubMed
Gasparo, M., Catt, K. J., Inagami, T., Wright, J. W. and Unger, T. (2000). The angiotensin II receptors. Pharmacol. Rev., 52, 415–72.Google ScholarPubMed
Dechend, R., Homuth, V., Wallukat, G., et al. (2000). AT1 receptor agonistic antibodies from preeclamptic patients cause vascular cells to express tissue factor. Circulation, 101, 2382–7.CrossRefGoogle Scholar
Dechend, R., Viedt, C., Muller, D. N., et al. (2003). AT1 receptor agonistic antibodies from preeclamptic patients stimulate NADPH oxidase. Circulation, 107, 1632–9.CrossRefGoogle ScholarPubMed
Dzau, V. J., Burt, D. W. and Pratt, R. E. (1988). Molecular biology of the renin–angiotensin system. Am. J. Physiol. Renal, Fluid Electro. Physiol., 255, F563–73.CrossRefGoogle ScholarPubMed
Ferrario, C. (2002). Angiotensin I, angiotensin II and their biologically active peptides. J. Hypertens., 20, 805–7.CrossRefGoogle ScholarPubMed
Ferrario, C. M., Chappell, M. C., Tallant, E. A., Brosnihan, K. B. and Diz, D. I. (1997). Counterregulatory actions of angiotensin-(1–7). Hypertension, 30, 535–41.CrossRefGoogle Scholar
Fruitier-Arnaudin, I., Cohen, M., Bordenave, S., Sannier, F. and Piot, J. M. (2002). Comparative effects of angiotensin IV and two hemorphins on angiotensin-converting enzyme activity. Peptides, 23, 1465–70.CrossRefGoogle ScholarPubMed
Fu, M. L., Herlitz, H., Schulze, W., et al. (2000). Autoantibodies against the angiotensin receptor (AT1) in patients with hypertension. J. Hypertens., 18, 945–53.CrossRefGoogle ScholarPubMed
Gallery, E. D., Stokes, G. S., Gyory, A. Z., Rowe, J. and Williams, J. (1980). Plasma renin activity in normal human pregnancy and in pregnancy-associated hypertension, with reference to cryoactivation. Clin. Sci., 59, 49–53.CrossRefGoogle ScholarPubMed
Gordon, R. D., Parsons, S. and Symonds, E. M. (1969). A prospective study of plasma-renin activity in normal and toxaemic pregnancy. Lancet, i(7590), 347–9.CrossRefGoogle Scholar
Gordon, R. D., Symonds, E. M., Wilmshurst, E. G. and Pawsey, C. G. (1973). Plasma renin activity, plasma angiotensin and plasma and urinary electrolytes in normal and toxaemic pregnancy, including a prospective study. Clin. Sci., 45, 115–27.CrossRefGoogle ScholarPubMed
Guo, G., Wilton, A. N., Fu, Y., Qiu, H., Brennecke, S. P. and Cooper, D. W. (1997). Angiotensinogen gene variation in a population case-control study of preeclampsia/eclampsia in Australians and Chinese. Electrophoresis, 18, 1646–9.CrossRefGoogle Scholar
Hagemann, A., Nielsen, A. H. and Poulsen, K. (1994). The uteroplacental renin–angiotensin system: a review. Exp. Clin. Endocrinol., 102(3), 252–61.CrossRefGoogle ScholarPubMed
Hanna, I. R., Taniyama, Y., Szocs, K., Rocic, P. and Griendling, K. K. (2002). NAD(P)H oxidase-derived reactive oxygen species as mediators of angiotensin II signaling. Antioxid. Redox. Signal., 4, 899–914.CrossRefGoogle ScholarPubMed
Hanssens, M., Keirse, M. J., Spitz, B. and Assche, F. A. (1991a). Angiotensin II levels in hypertensive and normotensive pregnancies. Br. J. Obstet. Gynaecol., 98, 155–61.CrossRefGoogle Scholar
Hanssens, M., Keirse, M. J. N. C., Spitz, B. and Assche, F. A. (1991b). Measurement of individual plasma angiotensins in normal pregnancy and pregnancy-induced hypertension. J. Clin. Endocrinol. Metab., 73, 489–94.CrossRefGoogle Scholar
Hayashi, R. H., Becker, R. A., Evans, G. T., Morris, K. and Franks, R. C. (1977). Prospective study of angiotensin II response to positional change in pregnancy-induced hypertension. Am. J. Obstet. Gynecol., 128, 872–8.CrossRefGoogle ScholarPubMed
Heiskanen, J. T., Pirskanen, M. M., Hiltunen, M. J., Mannermaa, A. J., Punnonen, K. R. and Heinonen, S. T. (2001). Insertion–deletion polymorphism in the gene for angiotensin-converting enzyme is associated with obstetric cholestasis but not with preeclampsia. Am. J. Obstet. Gynecol., 185, 600–3.CrossRefGoogle Scholar
Horio, J., Nomura, S., Okada, M., et al. (1999). Structural organization of the 5′-end and chromosomal assignment of human placental leucine aminopeptidase/insulin-regulated membrane aminopeptidase gene. Biochem. Biophys. Res. Commun., 262, 269–74.CrossRefGoogle ScholarPubMed
Ino, K., Uehara, C., Kikkawa, F., et al. (2003). Enhancement of aminopeptidase A expression during angiotensin II-induced choriocarcinoma cell proliferation through AT1 receptor involving protein kinase C- and mitogen-activated protein kinase-dependent signaling pathway. J. Clin. Endocrinol. Metab., 88, 3973–82.CrossRefGoogle ScholarPubMed
Inoue, I., Nakajima, T., Williams, C. S., et al. (1997). A nucleotide substitution in the promoter of human angiotensinogen is associated with essential hypertension and affects basal transcription in vitro. J. Clin. Invest., 99, 1786–97.CrossRefGoogle ScholarPubMed
Jikihara, H., Poisner, A. M., Hirsch, R. and Handwerger, S. (1995). Human uterine decidual macrophages express renin. J. Clin. Endocrinol. Metab., 80, 1273–7.Google ScholarPubMed
Johnson, A. R., Skidgel, R. A., Gafford, J. T. and Erdos, E. G. (1984). Enzymes in placental microvilli: angiotensin I converting enzyme, angiotensinase A, carboxypeptidase, and neutral endopeptidase (“enkephalinase”). Peptides, 5, 789–96.CrossRefGoogle Scholar
Johnson, I. R. (1980). Renin substrate, active and acid-activatable renin concentrations in human plasma and endometrium during the normal menstrual cycle. Br. J. Obstet. Gynaecol., 87, 875–82.CrossRefGoogle ScholarPubMed
Kaaja, R. J., Moore, M. P., Yandle, T. G., Ylikorkala, O., Frampton, C. M. and Nicholls, M. G. (1999). Blood pressure and vasoactive hormones in mild preeclampsia and normal pregnancy. Hypertens. Pregn., 18, 173–87.CrossRefGoogle ScholarPubMed
Keidar, S., Heinrich, R., Kaplan, M. and Aviram, M. (2002). Oxidative stress increases the expression of the angiotensin-II receptor type 1 in mouse peritoneal macrophages. J. Renin Angiotensin Aldosterone Syst., 3, 24–30.CrossRefGoogle ScholarPubMed
Kerins, D. M., Hao, Q. and Vaughan, D. E. (1995). Angiotensin induction of PAI-1 expression in endothelial cells is mediated by the hexapeptide angiotensin IV. J. Clin. Invest., 96, 2515–20.CrossRefGoogle ScholarPubMed
Kikkawa, F., Kajiyama, H., Ino, K., et al. (2002). Possible involvement of placental peptidases that degrade gonadotropin-releasing hormone (GnRH) in the dynamic pattern of placental hCG secretion via GnRH degradation. Placenta, 23, 483–9.CrossRefGoogle ScholarPubMed
Klickstein, L. B., Kaempfer, C. E. and Wintroub, B. U. (1982). The granulocyte–angiotensin system. Angiotensin I-converting activity of cathepsin G. J. Biol. Chem., 257, 15,042–6.Google ScholarPubMed
Knock, G. A., Sullivan, M. H., McCarthy, A., Elder, M. G., Polak, J. M. and Wharton, J. (1994). Angiotensin II (AT1) vascular binding sites in human placentae from normal-term, preeclamptic and growth retarded pregnancies. J. Pharmacol. Exp. Therap., 271, 1007–15.Google ScholarPubMed
Kobashi, G., Shido, K., Hata, A., et al. (2001). Multivariate analysis of genetic and acquired factors; T235 variant of the angiotensinogen gene is a potent independent risk factor for preeclampsia. Semin. Thromb. Hemost., 27, 143–7.CrossRefGoogle ScholarPubMed
Leung, P. S., Tsai, S. J., Wallukat, G., Leung, T. N. and Lau, T. K. (2001). The upregulation of angiotensin II receptor AT1 in human preeclamptic placenta. Molec. Cell. Endocrinol., 184, 95–102.CrossRefGoogle Scholar
Lever, A. F. (1993). Slow developing pressor effect of angiotensin II and vascular structure. J. Hypertens., 11(Suppl.), S27–8.Google ScholarPubMed
Li, P., Chappell, M. C., Ferrario, C. M. and Brosnihan, K. B. (1997). Angiotensin-(1–7) augments bradykinin-induced vasodilation by competing with ACE and releasing nitric oxide. Hypertension, 29, 394–400.CrossRefGoogle ScholarPubMed
Li, X. F. and Ahmed, A. (1996). Dual role of angiotensin II in the human endometrium. Hum. Reprod., 11, 95–108.CrossRefGoogle ScholarPubMed
Li, X. M., Moutquin, J. M., Deschenes, J., Bourque, L., Marois, M. and Forest, J. C. (1995). Increased immunohistochemical expression of neutral metalloendopeptidase (enkephalinase; EC 3.4.24.11) in villi of the human placenta with pre-eclampsia. Placenta, 16, 435–45.CrossRefGoogle ScholarPubMed
Lobov, I. B., Brooks, P. C. and Lang, R. A. (2002). Angiopoietin-2 displays VEGF-dependent modulation of capillary structure and endothelial cell survival in vivo. Proc. Natl Acad. Sci. USA, 99, 11,205–10.CrossRefGoogle ScholarPubMed
Merrill, D. C., Karoly, M., Chen, K., Ferrario, C. M. and Brosnihan, K. B. (2002). Angiotensin-(1–7) in normal and preeclamptic pregnancy. Endocrine J., 18, 239–45.CrossRefGoogle ScholarPubMed
Mizutani, S. and Tomoda, Y. (1996). Effects of placental proteases on maternal and fetal blood pressure in normal pregnancy and preeclampsia. Am. J. Hypertens., 9, 591–7.CrossRefGoogle ScholarPubMed
Moeller, I., Clune, E. F., Fennessy, P. A., et al. (1999). Up regulation of AT4 receptor levels in carotid arteries following balloon injury. Regul. Peptides, 83, 25–30.CrossRefGoogle ScholarPubMed
Morgan, L., Crawshaw, S., Baker, P. N., Edwards, R., Broughton Pipkin, F. and Kalsheker, N. (1997a). Functional and genetic studies of the angiotensin II type 1 receptor in pre-eclamptic and normotensive pregnant women. J. Hypertens., 15, 1389–96.CrossRefGoogle Scholar
Morgan, T., Craven, C., Nelson, L., Lalouel, J. M. and Ward, K. (1997b). Angiotensinogen T235 expression is elevated in decidual spiral arteries. J. Clin. Invest., 100, 1406–15.CrossRefGoogle Scholar
Morgan, T., Craven, C. and Ward, K. (1998). Human spiral artery renin–angiotensin system. Hypertension, 32, 683–7.CrossRefGoogle ScholarPubMed
Morgan, L., Crawshaw, S., Baker, P. N., Broughton Pipkin, F. and Kalsheker, N. (1999a). Maternal and fetal angiotensinogen gene allele sharing in pre-eclampsia. Br. J. Obstet. Gynaecol., 106, 244–51.CrossRefGoogle Scholar
Morgan, L., Foster, F., Hayman, R., et al. (1999b). Angiotensin-converting enzyme insertion–deletion polymorphism in normotensive and pre-eclamptic pregnancies. J. Hypertens., 17, 765–8.CrossRefGoogle Scholar
Morgan, T., Craven, C., Lalouel, J. M. and Ward, K. (1999c). Angiotensinogen Thr235 variant is associated with abnormal physiologic change of the uterine spiral arteries in first-trimester decidua. Am. J. Obstet. Gynecol., 180, 95–102.CrossRefGoogle Scholar
Nadal, J. A., Scicli, G. M., Carbini, L. A. and Scicli, A. G. (2002). Angiotensin II stimulates migration of retinal microvascular pericytes: involvement of TGF-beta and PDGF-BB. Am. J. Physiol. Heart Circ. Physiol., 282, H739–48.CrossRefGoogle ScholarPubMed
Neudeck, H., Schuster, C., Hildebrandt, R., et al. (1996). Histochemical evaluation of placental angiotensinase A in pre-eclampsia: enzyme activity in villous trophoblast indicates an enhanced likelihood of gestational proteinuric hypertension. Placenta, 17, 155–63.CrossRefGoogle ScholarPubMed
Oats, J. N., Broughton Pipkin, F., Symonds, E. M. and Craven, D. J. (1981). A prospective study of plasma angiotensin-converting enzyme in normotensive primigravidae and their infants. Br. J. Obstet. Gynaecol., 88, 1204–10.CrossRefGoogle ScholarPubMed
Otani, A., Takagi, H., Suzuma, K. and Honda, Y. (1998). Angiotensin II potentiates vascular endothelial growth factor-induced angiogenic activity in retinal microcapillary endothelial cells. Circ. Res., 82, 619–28.CrossRefGoogle ScholarPubMed
Otani, A., Takagi, H., Oh, H., Koyama, S. and Honda, Y. (2001). Angiotensin II induces expression of the Tie2 receptor ligand, angiopoietin-2, in bovine retinal endothelial cells. Diabetes, 50, 867–75.CrossRefGoogle ScholarPubMed
Page, E. L., Robitaille, G. A., Pouyssegur, J. and Richard, D. (2002). Induction of hypoxia-inducible factor-1alpha by transcriptional and translational mechanisms. J. Biol. Chem., 277, 48,403–9.CrossRefGoogle ScholarPubMed
Poulsen, K. and Jacobsen, J. (1993). Enzymic reactions of the renin–angiotensin system. In The Renin–Angiotensin System, vol. 1. ed. Robertson, J. I. S. and Nicholls, M. G., London: Gower Medical Publishing, pp. 5.1–5.12.Google Scholar
Rasmussen, A. B., Pedersen, E. B., Romer, F. K., et al. (1983). The influence of normotensive pregnancy and pre-eclampsia on angiotensin-converting enzyme. Acta Obstet. Gynecol. Scand., 62, 341–4.CrossRefGoogle ScholarPubMed
Richard, D. E., Berra, E. and Pouyssegur, J. (2000). Nonhypoxic pathway mediates the induction of hypoxia-inducible factor 1alpha in vascular smooth muscle cells. J. Biol. Chem., 275, 26,765–71.Google ScholarPubMed
Rigat, B., Hubert, C., Alhenc-Gelas, F., Cambien, F., Corvol, P. and Soubrier, F. (1990). An insertion/deletion polymorphism in the angiotensin I-converting enzyme gene accounting for half the variance of serum enzyme levels. J. Clin. Invest., 86, 1343–6.CrossRefGoogle ScholarPubMed
Ruilope, L., Paya, C., Alcazar, J. M., et al. (1984). Failure of angiotensin II to reduce plasma renin activity in hypertensive pregnant women. J. Hypertens., 2, S251–4.Google ScholarPubMed
Santos, R. A., Simoes e Silva, A. C., Maric, C., et al. (2003). Angiotensin-(1–7) is an endogenous ligand for the G protein-coupled receptor Mas. Proc. Natl Acad. Sci. USA, 100, 8258–63.CrossRefGoogle ScholarPubMed
Sethi, A. A., Nordestgaard, B. G. and Tybjaerg-Hansen, A. (2003). Angiotensinogen gene polymorphism, plasma angiotensinogen, and risk of hypertension and ischemic heart disease: a meta-analysis. Arterioscl. Thromb. Vasc. Biol., 23, 1269–75.CrossRefGoogle ScholarPubMed
Shah, D. M., Banu, J. M., Chirgwin, J. M. and Tekmal, R. R. (2000). Reproductive tissue renin gene expression in preeclampsia. Hypertens. Pregn., 19, 341–51.CrossRefGoogle ScholarPubMed
Skinner, S. L. (1993). The renin system in fertility and normal human pregnancy. In The Renin–Angiotensin System, vol. 1. ed. Robertson, J. I. S. N. and Nicholls, M. G., London: Gower Medical Publishing, pp. 50.1–50.16.Google Scholar
Skinner, S. L., Lumbers, E. R. and Symonds, E. M. (1972). Analysis of changes in the renin–angiotensin system during pregnancy. Clin. Sci., 42, 479–88.CrossRefGoogle ScholarPubMed
Sowers, J. R., Eggena, P., Kowal, D. K., Simpson, L., Zhu, J.-H. and Barrett, J. D. (1993). Expression of renin and angiotensinogen genes in preeclamptic and normal human placental tissue. Hypertens. Pregn., 12, 163–71.CrossRefGoogle Scholar
Strawn, W. B. and Ferrario, C. M. (2002). Mechanisms linking angiotensin II and atherogenesis. Curr. Opin. Lipidol., 13, 505–12.CrossRefGoogle ScholarPubMed
Suzuki, Y., Tanemura, M., Suzuki, Y., Murakami, I. and Suzumori, K. (1999). Is angiotensinogen gene polymorphism associated with hypertension in pregnancy?Hypertens. Pregn., 18, 261–71.CrossRefGoogle ScholarPubMed
Symonds, E. M. and Andersen, G. J. (1974). The effect of bed rest on plasma renin in hypertensive disease of pregnancy. J. Obstet. Gynaecol. Br. Commonwlth, 81, 676–81.CrossRefGoogle ScholarPubMed
Symonds, E. M., Stanley, M. A. and Skinner, S. L. (1968). Production of renin by in vitro cultures of human chorion and uterine muscle. Nature, 217, 1152–3.CrossRefGoogle ScholarPubMed
Symonds, E. M., Broughton Pipkin, F. and Craven, D. J. (1975). Changes in the renin-angiotensin system in primigravidae with hypertensive disease of pregnancy. Br. J. Obstet. Gynaecol., 82, 643–50.CrossRefGoogle ScholarPubMed
Tamura, T., Johanning, G. L., Goldenberg, R. L., Johnston, K. E. and DuBard, M. B. (1996). Effect of angiotensin-converting enzyme gene polymorphism on pregnancy outcome, enzyme activity, and zinc concentration. Obstet. Gynecol., 88, 497–502.CrossRefGoogle ScholarPubMed
Tewksbury, D. A., Kaiser, S. J. and Burrill, R. E. (2001). A study of the temporal relationship between plasma high molecular weight angiotensinogen and the development of pregnancy-induced hypertension. Am. J. Hypertens., 14, 794–7.CrossRefGoogle ScholarPubMed
Tigerstedt, R. and Bergman, P. (1898). Niere und Kreislauf. Skandi. Archiv Physiol., 8, 223–71.CrossRefGoogle Scholar
Tulenko, T. N. (1979). Regional sensitivity to vasoactive polypeptides in the human umbilicoplacental vasculature. Am. J. Obstet. Gynecol., 135, 629–36.CrossRefGoogle ScholarPubMed
Valdes, G., Germain, A. M., Corthorn, J., et al. (2001). Urinary vasodilator and vasoconstrictor angiotensins during menstrual cycle, pregnancy, and lactation. Endocrine J., 16, 117–22.CrossRefGoogle ScholarPubMed
Viinikainen, A., Nyman, T., Fyhrquist, F. and Saijonmaa, O. (2002). Downregulation of angiotensin converting enzyme by TNF-alpha in differentiating human macrophages. Cytokine, 18(6), 304–10.CrossRefGoogle ScholarPubMed
Wallukat, G., Homuth, V., Fischer, T., et al. (1999). Patients with preeclampsia develop agonistic autoantibodies against the angiotensin AT1 receptor. J. Clin. Invest., 103, 945–52.CrossRefGoogle ScholarPubMed
Ward, K., Hata, A., Jeunemaitre, X., et al. (1993). A molecular variant of angiotensinogen associated with preeclampsia. Nature Genet., 4, 59–61.CrossRefGoogle ScholarPubMed
Williams, B., Baker, A. Q., Gallacher, B. and Lodwick, D. (1995). Angiotensin II increases vascular permeability factor gene expression by human vascular smooth muscle cells. Hypertension, 25, 913–17.CrossRefGoogle ScholarPubMed
Xia, Y., Wen, H., Bobst, S., Day, M. C. and Kellems, R. E. (2003). Maternal autoantibodies from preeclamptic patients activate angiotensin receptors on human trophoblast cells. J. Soc. Gynecol. Invest., 10, 82–93.CrossRefGoogle ScholarPubMed
Xia, Y., Wen, H. Y. and Kellems, R. E. (2002). Angiotensin II inhibits human trophoblast invasion through AT1 receptor activation. J. Biol. Chem., 277, 24,601–8.CrossRefGoogle ScholarPubMed
Yamahara, N., Nomura, S., Suzuki, T., et al. (2000). Placental leucine aminopeptidase/oxytocinase in maternal serum and placenta during normal pregnancy. Life Sci., 66, 1401–10.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×