Murine Pre-Eclampsia Induced by Unspecific Activation of the Immune System Correlates with Alterations in the eNOS and AT1 Receptor Expression in the Kidneys and Placenta

Placenta

Volumn 28, Issue 7, 2007, Pages 688-700

  Schmid, M ^a   Sollwedel, A ^a   Thuere, C ^a   Wafula, P O ^a   Zenclussen, M L ^a   Muller D N ^b   Gratze, P ^b   Woiciechowsky, C ^a   Volk, H D ^a   Zenclussen, A C ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

AT1R; eNOS; Hypertension; Murine model; Pre eclampsia; Th1 cell

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN 2 RECEPTOR; ANGIOTENSIN II; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 12; INTERLEUKIN 2; MESSENGER RNA; NITRIC OXIDE;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE REGULATION; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; FETOPLACENTAL UNIT; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; IMMUNOSTIMULATION; KIDNEY PARENCHYMA; LABOR INDUCTION; LYMPHOCYTE CULTURE; MOUSE; NONHUMAN; PATHOGENESIS; PLACENTA; PREECLAMPSIA; PREGNANCY OUTCOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION; TH1 CELL; UPREGULATION;

ADOPTIVE TRANSFER; ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; IMMUNE SYSTEM; KIDNEY; MICE; MICE, INBRED STRAINS; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; RECEPTOR, ANGIOTENSIN, TYPE 1; RECEPTOR, ANGIOTENSIN, TYPE 2; RNA, MESSENGER; TH1 CELLS; UP-REGULATION;

EID: 34249785927     PISSN: 01434004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.placenta.2006.10.008     Document Type: Article

References (48)

1. Robillard P.Y. Interest in preeclampsia for researchers in reproduction. J Reprod Immunol. 53 (2002) 279-287
2. Pijnenborg R., Luyten C., Vercruysse L., and Van Assche F.A. Attachment and differentiation in vitro of trophoblast from normal and preeclamptic human placentas. Am J Obstet Gynecol. 175 (1996) 30-36
3. Zhou Y., Damsky C., and Fisher S. Pre-eclampsia is associated with failure of human cytotrophoblasts to mimic a vascular adhesion phenotype. J Clin Invest. 99 (1999) 2152-2164
4. von Dadelszen P., and Magee L.A. Could an infectious trigger explain the differential maternal response to the shared placental pathology of preeclampsia and normotensive intrauterine growth restriction?. Acta Obstet Gynecol Scand 81 (2002) 642-648
5. Redman C.W.G., Sacks G.P., and Sargent I.L. Preeclampsia: An excessive maternal inflammatory response to pregnancy. Am J Obstet Gynecol. 180 (1999) 499-506
6. Roberts J.M., Taylor R.N., and Goldfien A. Clinical and biochemical evidence of endothelial cell dysfunction in the pregnancy syndrome preeclampsia. Am. J Hypertens 8 (1991) 700-708
7. Faas M.M., Schuiling G., Baller J.F.W., Visscher C.A., and Bakker W.W. A new animal model for human preeclampsia: ultralow dose endotoxin infusion in pregnant rats. Am J Obstet Gynecol. 171 (1994) 158-164
8. Faas M.M., and Schuiling G.A. Pre-eclampsia and the inflammatory response. Eur. J Obstet Gynecol Reprod Biol. 95 (2001) 213-217
9. Saito S., Umekage H., Sakamoto Y., Sakai M., Tanebe K., Sasaki Y., et al. Increased T-helper-1-type immunity and decreased T-helper-2-type immunity in patients with preeclampsia. Am J Reprod Immunol. 5 (1999) 297-306
10. Sacks G.P., Studena K., Sargent I.L., and Redman C.W. CD11b expression on circulating neutrophils in pre-eclampsia. Clin Sci. 93 (1997) 187-189
11. Oian P., Omsjo I., Maltau J.M., and Osterud B. Increased sensitivity to thromboplastin synthesis in blood monocytes from pre-eclamptic patients. Br J Obstet Gynaecol. 92 (1985) 511-517
12. Greer I.A., Haddad N.G., Dawes J., Johnstone F.D., and Calder A.A. Neutrophil activation in pregnancy-induced hypertension. Br J Obstet Gynaecol. 96 (1989) 978-982
13. Darmochwal-Kolarz D., Leszczynska-Gorzelak B., Rolinski J., and Oleszczuk J. T helper 1- and T helper 2-type cytokine imbalance in pregnant women with pre-eclampsia. Eur J Obstet Gynecol Reprod Biol. 86 (1999) 165-170
14. Stark J.M. Pre-eclampsia and cytokine induced oxidative stress. Br J Obstet Gynaecol. 100 (1993) 105-109
15. Zenclussen A., Fest S., Joachim R., Klapp B., and Arck P. Introducing a mousemodel for pre-eclampsia: adoptive transfer of activated Th1 cells leads to pre-eclamspia-like symptoms exclusively in pregnant mice. Eur J Immunol. 24 (2004) 377-387
16. Dudzinski D.M., Igarashi J., Greif D., and Michel T. The regulation and pharmacology of endothelial nitric oxide synthase. Annu Rev Pharmacol Toxicol. 46 (2006) 235-276
17. Myatt L., Eis A.L., Brockman D.E., Kossenjans W., Greer I., and Lyall F. Inducible (type II) nitric oxide Synthase in human placental villous tissue of normotensive, pre-eclamptic and intrauterine growth-restricted pregnancies. Placenta 18 (1997) 261-268
18. Berdeaux A. Nitric oxide: an ubiquitous messenger. Fundam Clin Pharmacol. 7 (1993) 401-411
19. Kashiwagi M., Zimmermann R., and Beinder E. Pathophysiology of pre-eclampsia: update on the role of nitric oxide. Curr Hypertens Rep. 5 6 (2003) 493-497
20. Kuriyama H., Kitamura K., Itoh T., and Inoue R. Physiological features of visceral smooth muscle cells, with special reference to receptors and ion channels. Physiol Rev. 78 (1998) 811-920
21. Napoletano M., Miceli F., Calce A., Vacca A., Gulino A., Apa R., et al. Expression and relationship between endothelin-1 messenger ribonucleic acid (mRNA) and inducible/endothelial nitric oxide synthase mRNA isoforms from normal and preeclamptic placentas. J Clin Endocrinol Metab. 85 6 (2000) 2318-2323
22. Murakami K., and Fukamizu A. Transgenic and knockout models in renin-angiotensin system. Immunopharmacology 44 (1999) 1-7
23. Reid I.A., Morris B.J., and Ganong W.F. The renin-angiotensin system. Annu Rev Physiol. 40 (1978) 377-410
24. Roberts J.M., Taylor R.N., Musci T.J., Rodgers G.M., Hubel C.A., and McLaughlin M.K. Preeclampsia: an endothelial cell disorder. Am J Obstet Gynecol. 161 (1989) 1200
25. Baylis C., and Engels K. Adverse interactions between pregnancy and a new model of systemic hypertension produced by chronic blockade of endothelial derived relaxing factor (EDRF) in the rat. Clin Exp Hypertens 11 (1992) 117
26. Molnar M., Sütö T., Toth T., and Hertelendy F. Prolonged blockade of nitric oxide synthesis in gravid rats produces sustained hypertension, proteinuria. thrombocytopenia and intrauterine growth retardation. Am J Obstet Gynecol. 170 (1994) 1458
27. Yallampalli C., and Garfield R.E. Inhibition of nitric oxide synthesis in rats during pregnancy produces signs similar to those of preeclampsia. Am J Obstet Gynecol. 169 (1993) 1316
28. Sainte-Marie G. A paraffin embedding technique for studies employing immunofluorescence. J. Histochem Cytochem. 10 (1962) 250-256
29. Zenclussen A.C., Sollwedel A., Bertoja A.Z., Gerlof K., Zenclussen M.L., Woiciechowsky C., et al. Heme oxygenase as a therapeutic target in immunological pregnancy complications. Int Immunopharmacol. 5 1 (2005) 41-51
30. Dechend R., Gratze P., Wallukat G., Shagdarsuren E., Plehm R., Brasen J.H., et al. Agonistic autoantibodies to the AT1 receptor in a transgenic rat model of preeclampsia. Hypertension 45 (2005) 742-746
31. Hayakawa S., Fujikawa T., Fukuoka H., Chisima F., Karasaki-Suzuki M., Ohkoshi E., et al. Murine fetal resorption and experimental pre-eclampsia are induced by both excessive Th1 and Th2 activation. J Reprod Immunol. 47 (2000) 121-138
32. Goetz R.M., Morano I., Calovini T., Studer R., and Holtz J. Increased expression of endothelial constitutive nitric oxide synthase in rat aorta during pregnancy. Biochem Biophys Res Commun. 205 (1994) 905-910
33. Weiner C.P., Lizasoain I., Baylis S.A., Knowles R.G., Charles I.G., and Moncada S. Induction of calcium-dependent nitric oxide synthases by sex hormones. Proc Natl Acad Sci USA 91 (1994) 5212-5216
34. Xu D.-L., Martin P.-Y., St. John J., Tsai P., Summer S.N., Ohara M., et al. Upregulation of endothelial and neuronal constitutive nitric oxide synthase in pregnant rats. Am J Physiol Regul Integr Comp Physiol. 271 (1996) R1739-R1745
35. Dötsch J., Hogen N., Nyùl Z., Hänze J., Knerr I., Kirschbaum M., et al. Increase of endothelial nitric oxide synthase and endothelin-1 mRNA expression in human placenta during gestation. Eur J Obstet Gynecol Reprod Biol. 97 (2001) 163-167
36. Faxén M., Nissel H., and Kublickiene K.-R. Altered mRNA expression of eNOS and iNOS in myometrium and placenta from women with preeclampsia. Arch Gynecol Obstet. 256 (2001) 45-50
37. Napolitano M., Miceli F., Calce A., Vacca A., Gulino A., Apa R., et al. Expression and relationship between Endothelin-1 messenger ribonucleic acid (mRNA) and inducible/endothelial nitric oxide synthase mRNA isoforms from normal and preeclamptic placentas. J Clin Endocrinol Metab. 85 6 (2000) 2318-2323
38. Karteris E., Vatish M., Hillhouse E.W., and Grammatopoulos D.K. Preeclampsia is associated with impaired regulation of the placental nitric oxide-cGMP pathway by CRH and CRH-related peptides. J Clin Endocrinol Metab. 10 (2005) 2004-2210
39. Morris N.H., Sooranna S.R., Learmont J.G., Poston L., Ramsey B., Pearson J.D., et al. Nitric oxide Synthase activities in placental tissue from normotensive, pre-eclamptic and growth retarted pregnancies. Br J Obstet Gynaecol. 102 (1995) 711-714
40. Fitzgerald D.J., Entmann S.S., Mulloy K., and Fitzgerald G.A. Decreased prostacyclin biosynthesis preceding the clinical manifestation of pregnancy-induced hypertension. Circulation 75 (1987) 956-963
41. Bunting S.R., Gryglewski R., Moncada A.S., and Vane J.R. Arterial walls generate from prostaglandin endoperoxides a substance (prostaglandin X) which relaxes strips of mesenteric and celiac arteries and inhibits platelet aggregation. Prostaglandins 12 (1976) 897-913
42. Timmermans P., Wong P.C., Chiu A.T., Herblin W.F., Benfield P., Carini D.J., et al. Angiotensin II receptors and angiotensin II receptor antagonists. Pharmacol Rev. 45 (1993) 205-251
43. August P., Lenz P., Ales K.L., Druzin M.I., Edersheim T.G., Hutson J.M., et al. Longitudinal study of the renin-angiotensin-aldosterone system in hypertensive pregnant women: Deviations related to the development of superimposed preeclampsia. Am J Obstet Gynecol. 163 (1990) 1612-1621
44. Leung P.S., Tsai S.J., Wallukat G., Leung T.N., and Lau T.K. The upregulation of angiotensin II receptor AT(1) in human preeclamptic placenta. Mol Cell Endocrinol. 184 1-2 (2001) 95-102
45. Wallukat G., Homuth V., Fischer T., Lindschau C., Horstkamp B., Jupner A., et al. Patients with preeclampsia develop agonistic autoantibodies against the angiotensin AT1 receptor. J Clin Invest. 103 7 (1999) 945-952
46. Dechend R., Viedt C., Muller D.N., Ugele B., Brandes R.P., Wallukat G., et al. AT1 receptor agonistic antibodies from preeclamptic patients stimulate NADPH oxidase. Circulation 107 12 (2003) 1632-1639
47. Thyway T.M., Shlykov S.G., Day M.C., Sanborn B.M., Gilstrap L.C., Xia Y., et al. Antibodies from preeclamptic patients stimulate increased intracellular Ca2 + mobilization through angiotensin receptor activation. Circulation 110 12 (2004) 1612-1619
48. Itoh T., Kajikuri J., Tada T., Suzuki Y., and Mabuchi Y. Angiotensin II-induced modulation of endothelium-dependent relaxation in rabbit mesenteric resistance arteries. J Physiol. 548 (2003) 893-906