A potential pathophysiological role for galectins and the renin-angiotensin system in preeclampsia

Cellular and Molecular Life Sciences

Volumn 72, Issue 1, 2015, Pages 39-50

  Blois, Sandra M ^a   Dechend, Ralf ^b   Barrientos, Gabriela ^c   Staff, Anne Cathrine ^d  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b HELIOS KLINIKUM BERLIN BUCH   (Germany)

^c HOSPITAL ALEMÁN   (Argentina)

^d OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

Acute atherosis; Galectins; Preeclampsia; Renin angiotensin system

Indexed keywords

ENDOGLIN; GALECTIN; GALECTIN 1; GALECTIN 13; GALECTIN 3; PLACENTAL GROWTH FACTOR; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ACUTE ATHEROSIS; CARDIOVASCULAR DISEASE; CEREBROVASCULAR ACCIDENT; CORONARY ARTERY ATHEROSCLEROSIS; CYTOTROPHOBLAST; DIABETES MELLITUS; DISEASE SEVERITY; DYSLIPIDEMIA; ENDOPLASMIC RETICULUM STRESS; ENDOTHELIAL DYSFUNCTION; FAMILY HISTORY; HELLP SYNDROME; HUMAN; HYPERTENSION; IN VIVO STUDY; INSULIN RESISTANCE; ISCHEMIC HEART DISEASE; MATERNAL WELFARE; NONHUMAN; OBESITY; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PREECLAMPSIA; PREGNANCY; PREMATURE LABOR; PROTEIN EXPRESSION; PROTEINURIA; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REPERFUSION INJURY; REVIEW; RISK FACTOR; SIGNAL TRANSDUCTION; SMOKING; ANIMAL; FEMALE; METABOLISM; MOUSE; PHYSIOLOGY; RAT;

ANIMALIA; MUS; RATTUS;

ANIMALS; FEMALE; GALECTINS; HUMANS; MICE; PRE-ECLAMPSIA; PREGNANCY; RATS; RENIN-ANGIOTENSIN SYSTEM;

EID: 84920153905     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-014-1713-1     Document Type: Review

References (107)

1. Redman CW, Sargent IL (2005) Latest advances in understanding preeclampsia. Science 308(5728):1592-1594. doi:10.1126/science.1111726
2. Duley L (2009) The global impact of pre-eclampsia and eclampsia. Semin Perinatol 33(3):130-137. doi:10.1053/j.semperi.2009.02.010
3. Redman CW, Sargent IL (2010) Immunology of pre-eclampsia. Am J Reprod Immunol 63(6):534-543. doi:10.1111/j.1600-0897.2010.00831.x
4. Staff AC, Benton SJ, von Dadelszen P, Roberts JM, Taylor RN, Powers RW, Charnock-Jones DS, Redman CW (2013) Redefining preeclampsia using placenta-derived biomarkers. Hypertension 61(5):932-942. doi:10.1161/HYPERTENSIONAHA.111.00250
5. Staff AC, Johnsen GM, Dechend R, Redman CW (2014) Pre-eclampsia and uteroplacental acute atherosis: immune and inflammatory factors. J Reprod Immunol 101-102:120-126. doi:10.1016/j.jri.2013.09.001
6. Stevens DU, Al-Nasiry S, Bulten J, Spaanderman ME (2013) Decidual vasculopathy in preeclampsia: lesion characteristics relate to disease severity and perinatal outcome. Placenta 34(9):805-809. doi:10.1016/j.placenta.2013.05.008
7. Burton GJ, Woods AW, Jauniaux E, Kingdom JC (2009) Rheological and physiological consequences of conversion of the maternal spiral arteries for uteroplacental blood flow during human pregnancy. Placenta 30(6):473-482. doi:10.1016/j.placenta.2009.02.009
8. Staff AC, Dechend R, Pijnenborg R (2010) Learning from the placenta: acute atherosis and vascular remodeling in pre-eclampsia-novel aspects for atherosclerosis and future cardiovascular health. Hypertension 56(6):1026-1034. doi:10.1161/HYPERTENSIONAHA.110.157743
9. Redman CW, Sargent IL, Staff AC (2014) IFPA Senior Award Lecture: making sense of pre-eclampsia - two placental causes of preeclampsia? Placenta 35(Suppl):S20-25. doi:10.1016/j.placenta.2013.12.008
10. Maynard SE, Min JY, Merchan J, Lim KH, Li J, Mondal S, Libermann TA, Morgan JP, Sellke FW, Stillman IE, Epstein FH, Sukhatme VP, Karumanchi SA (2003) Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 111(5):649-658. doi:10.1172/JCI17189
11. Barondes SH, Castronovo V, Cooper DN, Cummings RD, Drickamer K, Feizi T, Gitt MA, Hirabayashi J, Hughes C, Kasai K et al (1994) Galectins: a family of animal beta-galactoside-binding lectins. Cell 76(4):597-598 pii:0092-8674(94)90498-7
12. Liu FT, Patterson RJ, Wang JL (2002) Intracellular functions of galectins. Biochim Biophys Acta 1572(2-3):263-273
13. Hernandez JD, Baum LG (2002) Ah, sweet mystery of death! Galectins and control of cell fate. Glycobiology 12(10):127R-136R
14. Nickel W (2005) Unconventional secretory routes: direct protein export across the plasma membrane of mammalian cells. Traffic 6(8):607-614 (Copenhagen, Denmark)
15. Rabinovich GA, Liu FT, Hirashima M, Anderson A (2007) An emerging role for galectins in tuning the immune response: lessons from experimental models of inflammatory disease, autoimmunity and cancer. Scand J Immunol 66(2-3):143-158
16. Hirabayashi J, Ayaki H, Soma G, Kasai K (1989) Cloning and nucleotide sequence of a full-length cDNA for human 14 kDa beta-galactoside-binding lectin. Biochim Biophys Acta 1008(1):85-91
17. Camby I, Le Mercier M, Lefranc F, Kiss R (2006) Galectin-1: a small protein with major functions. Glycobiology 16(11):137R-157R
18. Stillman BN, Hsu DK, Pang M, Brewer CF, Johnson P, Liu FT, Baum LG (2006) Galectin-3 and galectin-1 bind distinct cell surface glycoprotein receptors to induce T cell death. J Immunol 176(2):778-789
19. Blaser C, Kaufmann M, Muller C, Zimmermann C, Wells V, Mallucci L, Pircher H (1998) Beta-galactoside-binding protein secreted by activated T cells inhibits antigen-induced proliferation of T cells. Eur J Immunol 28(8):2311-2319
20. Motran CC, Molinder KM, Liu SD, Poirier F, Miceli MC (2008) Galectin-1 functions as a Th2 cytokine that selectively induces Th1 apoptosis and promotes Th2 function. Eur J Immunol 38(11):3015-3027
21. Blois SM, Ilarregui JM, Tometten M, Garcia M, Orsal AS, Cordo-Russo R, Toscano MA, Bianco GA, Kobelt P, Handjiski B, Tirado I, Markert UR, Klapp BF, Poirier F, Szekeres-Bartho J, Rabinovich GA, Arck PC (2007) A pivotal role for galectin-1 in fetomaternal tolerance. Nat Med 13(12):1450-1457
22. Tirado-Gonzalez I, Freitag N, Barrientos G, Shaikly V, Nagaeva O, Strand M, Kjellberg L, Klapp BF, Mincheva-Nilsson L, Cohen M, Blois SM (2013) Galectin-1 influences trophoblast immune evasion and emerges as a predictive factor for the outcome of pregnancy. Mol Hum Reprod 19(1):43-53
23. Choe YS, Shim C, Choi D, Lee CS, Lee KK, Kim K (1997) Expression of galectin-1 mRNA in the mouse uterus is under the control of ovarian steroids during blastocyst implantation. Mol Reprod Dev 48(2):261-266
24. von Wolff M, Wang X, Gabius HJ, Strowitzki T (2005) Galectin fingerprinting in human endometrium and decidua during the menstrual cycle and in early gestation. Mol Hum Reprod 11(3):189-194
25. Barrientos G, Freitag N, Tirado-Gonzalez I, Unverdorben L, Jeschke U, Thijssen VL, Blois SM (2014) Involvement of galectin-1 in reproduction: past, present and future. Human Repro Update 20(2):175-193
26. Bevan BH, Kilpatrick DC, Liston WA, Hirabayashi J, Kasai K (1994) Immunohistochemical localization of a beta-D-galactoside-binding lectin at the human maternofetal interface. Histochem J 26(7):582-586
27. Fischer I, Redel S, Hofmann S, Kuhn C, Friese K, Walzel H, Jeschke U (2010) Stimulation of syncytium formation in vitro in human trophoblast cells by galectin-1. Placenta 31(9):825-832
28. Kolundzic N, Bojić-Trbojević T, Kovaćević T, Stefanoska I, Kadoya T, Vićovac L (2011) Galectin-1 is part of human trophoblast invasion machinery: a functional study in vitro. PloS One 6(12):e28514
29. Aplin JD (1991) Implantation, trophoblast differentiation and haemochorial placentation: mechanistic evidence in vivo and in vitro. J Cell Sci 99(Pt 4):681-692
30. Hunt JS, Petroff MG, McIntire RH, Ober C (2005) HLA-G and immune tolerance in pregnancy. Faseb J 19(7):681-693
31. Thijssen VL, Barkan B, Shoji H, Aries IM, Mathieu V, Deltour L, Hackeng TM, Kiss R, Kloog Y, Poirier F, Griffioen AW (2010) Tumor cells secrete galectin-1 to enhance endothelial cell activity. Cancer Res 70(15):6216-6224
32. Hsieh SH, Ying NW, Wu MH, Chiang WF, Hsu CL, Wong TY, Jin YT, Hong TM, Chen YL (2008) Galectin-1, a novel ligand of neuropilin-1, activates VEGFR-2 signaling and modulates the migration of vascular endothelial cells. Oncogene 27(26):3746-3753
33. Douglas NC, Tang H, Gomez R, Pytowski B, Hicklin DJ, Sauer CM, Kitajewski J, Sauer MV, Zimmermann RC (2009) Vascular endothelial growth factor receptor 2 (VEGFR-2) functions to promote uterine decidual angiogenesis during early pregnancy in the mouse. Endocrinology 150(8):3845-3854
34. Halder JB, Zhao X, Soker S, Paria BC, Klagsbrun M, Das SK, Dey SK (2000) Differential expression of VEGF isoforms and VEGF(164)-specific receptor neuropilin-1 in the mouse uterus suggests a role for VEGF(164) in vascular permeability and angiogenesis during implantation. Genesis 26(3):213-224
35. Plaks V, Birnberg T, Berkutzki T, Sela S, BenYashar A, Kalchenko V, Mor G, Keshet E, Dekel N, Neeman M, Jung S (2008) Uterine DCs are crucial for decidua formation during embryo implantation in mice. J Clin Investig 118(12):3954-3965
36. Freitag N, Tirado-Gonzalez I, Barrientos G, Herse F, Thijssen VL, Weedon-Fekjaer SM, Schulz H, Wallukat G, Klapp BF, Nevers T, Sharma S, Staff AC, Dechend R, Blois SM (2013) Interfering with Gal-1-mediated angiogenesis contributes to the pathogenesis of preeclampsia. Proc Natl Acad Sci USA 110(28):11451-11456
37. Jeschke U, Mayr D, Schiessl B, Mylonas I, Schulze S, Kuhn C, Friese K, Walzel H (2007) Expression of galectin-1, -3 (gal-1, gal-3) and the Thomsen-Friedenreich (TF) antigen in normal, IUGR, preeclamptic and HELLP placentas. Placenta 28(11-12):1165-1173
38. Than NG, Erez O, Wildman DE, Tarca AL, Edwin SS, Abbas A, Hotra J, Kusanovic JP, Gotsch F, Hassan SS, Espinoza J, Papp Z, Romero R (2008) Severe preeclampsia is characterized by increased placental expression of galectin-1. J Matern Fetal Neonatal Med 21(7):429-442
39. Molvarec A, Blois SM, Stenczer B, Toldi G, Tirado-Gonzalez I, Ito M, Shima T, Yoneda S, Vasarhelyi B, Rigo J Jr, Saito S (2011) Peripheral blood galectin-1-expressing T and natural killer cells in normal pregnancy and preeclampsia. Clinical Immunol 139(1):48-56 (Orlando, Fla)
40. Brewer CF, Miceli MC, Baum LG (2002) Clusters, bundles, arrays and lattices: novel mechanisms for lectin-saccharide-mediated cellular interactions. Curr Opin Struct Biol 12(5):616-623
41. Vicovac L, Jankovic M, Cuperlovic M (1998) Galectin-1 and -3 in cells of the first trimester placental bed. Human Repro (Oxford, England) 13(3):730-735
42. Chen HY, Liu FT, Yang RY (2005) Roles of galectin-3 in immune responses. Archivum Immunologiae et Therapiae Experimentalis 53(6):497-504
43. Alves CM, Silva DA, Azzolini AE, Marzocchi-Machado CM, Carvalho JV, Pajuaba AC, Lucisano-Valim YM, Chammas R, Liu FT, Roque-Barreira MC, Mineo JR (2010) Galectin-3 plays a modulatory role in the life span and activation of murine neutrophils during early Toxoplasma gondii infection. Immunobiology 215(6):475-485
44. Iglesias MM, Rabinovich GA, Ambrosio AL, Castagna LF, Sotomayor CE, Wolfenstein-Todel C (1998) Purification of galectin-3 from ovine placenta: developmentally regulated expression and immunological relevance. Glycobiology 8(1):59-65
45. Yang RY, Hsu DK, Liu FT (1996) Expression of galectin-3 modulates T-cell growth and apoptosis. Proc Natl Acad Sci USA 93(13):6737-6742
46. Phillips B, Knisley K, Weitlauf KD, Dorsett J, Lee V, Weitlauf H (1996) Differential expression of two beta-galactoside-binding lectins in the reproductive tracts of pregnant mice. Biol Reprod 55(3):548-558
47. Yang H, Lei C, Zhang W (2012) Expression of galectin-3 in mouse endometrium and its effect during embryo implantation. Repro Biomed Online 24(1):116-122
48. Maquoi E, van den Brule FA, Castronovo V, Foidart JM (1997) Changes in the distribution pattern of galectin-1 and galectin-3 in human placenta correlates with the differentiation pathways of trophoblasts. Placenta 18(5-6):433-439
49. Lee VH, Lee AB, Phillips EB, Roberts JK, Weitlauf HM (1998) Spatio-temporal pattern for expression of galectin-3 in the murine utero-placental complex: evidence for differential regulation. Biol Reprod 58(5):1277-1282
50. Crider-Pirkle S, Billingsley P, Faust C, Hardy DM, Lee V, Weitlauf H (2002) Cubilin, a binding partner for galectin-3 in the murine utero-placental complex. J Biol Chem 277(18):15904-15912
51. Nangia-Makker P, Honjo Y, Sarvis R, Akahani S, Hogan V, Pienta KJ, Raz A (2000) Galectin-3 induces endothelial cell morphogenesis and angiogenesis. Am J Pathol 156(3):899-909
52. Fukushi J, Makagiansar IT, Stallcup WB (2004) NG2 proteoglycan promotes endothelial cell motility and angiogenesis via engagement of galectin-3 and alpha3beta1 integrin. Mol Biol Cell 15(8):3580-3590
53. Wan SY, Zhang TF, Ding Y (2011) Galectin-3 enhances proliferation and angiogenesis of endothelial cells differentiated from bone marrow mesenchymal stem cells. Transpl Proc 43(10):3933-3938
54. Machado CM, Andrade LN, Teixeira VR, Costa FF, Melo CM, dos Santos SN, Nonogaki S, Liu FT, Bernardes ES, Camargo AA, Chammas R (2014) Galectin-3 disruption impaired tumoral angiogenesis by reducing VEGF secretion from TGFbeta1-induced macrophages. Cancer Med 3(2):201-214
55. Markowska AI, Jefferies KC, Panjwani N (2011) Galectin-3 protein modulates cell surface expression and activation of vascular endothelial growth factor receptor 2 in human endothelial cells. J Biol Chem 286(34):29913-29921
56. D'Haene N, Sauvage S, Maris C, Adanja I, Le Mercier M, Decaestecker C, Baum L, Salmon I (2013) VEGFR1 and VEGFR2 involvement in extracellular galectin-1- and galectin-3-induced angiogenesis. PLoS One 8(6):e67029
57. Than NG, Sumegi B, Than GN, Berente Z, Bohn H (1999) Isolation and sequence analysis of a cDNA encoding human placental tissue protein 13 (PP13), a new lysophospholipase, homologue of human eosinophil Charcot-Leyden Crystal protein. Placenta 20(8):703-710
58. Than NG, Pick E, Bellyei S, Szigeti A, Burger O, Berente Z, Janaky T, Boronkai A, Kliman H, Meiri H, Bohn H, Than GN, Sumegi B (2004) Functional analyses of placental protein 13/galectin-13. Eur J Biochem/FEBS 271(6):1065-1078
59. Than NG, Romero R, Goodman M, Weckle A, Xing J, Dong Z, Xu Y, Tarquini F, Szilagyi A, Gal P, Hou Z, Tarca AL, Kim CJ, Kim JS, Haidarian S, Uddin M, Bohn H, Benirschke K, Santolaya-Forgas J, Grossman LI, Erez O, Hassan SS, Zavodszky P, Papp Z, Wildman DE (2009) A primate subfamily of galectins expressed at the maternal-fetal interface that promote immune cell death. Proc Natl Acad Sci USA 106(24):9731-9736
60. Kliman HJ, Sammar M, Grimpel YI, Lynch SK, Milano KM, Pick E, Bejar J, Arad A, Lee JJ, Meiri H, Gonen R (2012) Placental protein 13 and decidual zones of necrosis: an immunologic diversion that may be linked to preeclampsia. Repro Sci 19(1):16-30 (Thousand Oaks, Calif)
61. Gizurarson S, Huppertz B, Osol G, Skarphedinsson JO, Mandala M, Meiri H (2013) Effects of placental protein 13 on the cardiovascular system in gravid and non-gravid rodents. Fetal Diagn Ther 33(4):257-264
62. Than NG, Abdul Rahman O, Magenheim R, Nagy B, Fule T, Hargitai B, Sammar M, Hupuczi P, Tarca AL, Szabo G, Kovalszky I, Meiri H, Sziller I, Rigo J Jr, Romero R, Papp Z (2008) Placental protein 13 (galectin-13) has decreased placental expression but increased shedding and maternal serum concentrations in patients presenting with preterm pre-eclampsia and HELLP syndrome. Virchows Arch 453(4):387-400
63. Ogawa M, Yanoma S, Nagashima Y, Okamoto N, Ishikawa H, Haruki A, Miyagi E, Takahashi T, Hirahara F, Miyagi Y (2007) Paradoxical discrepancy between the serum level and the placental intensity of PP5/TFPI-2 in preeclampsia and/or intrauterine growth restriction: possible interaction and correlation with glypican-3 hold the key. Placenta 28(2-3):224-232
64. Sekizawa A, Purwosunu Y, Yoshimura S, Nakamura M, Shimizu H, Okai T, Rizzo N, Farina A (2009) PP13 mRNA expression in trophoblasts from preeclamptic placentas. Repro Sci Calif 16(4):408-413 (Thousand Oaks, Calif)
65. Huppertz B, Meiri H, Gizurarson S, Osol G, Sammar M (2013) Placental protein 13 (PP13): a new biological target shifting individualized risk assessment to personalized drug design combating pre-eclampsia. Human Repro Update 19(4):391-405
66. Nicolaides KH, Bindra R, Turan OM, Chefetz I, Sammar M, Meiri H, Tal J, Cuckle HS (2006) A novel approach to first-trimester screening for early pre-eclampsia combining serum PP-13 and Doppler ultrasound. Ultrasound Obstet Gynecol 27(1):13-17
67. Wortelboer EJ, Koster MP, Cuckle HS, Stoutenbeek PH, Schielen PC, Visser GH (2010) First-trimester placental protein 13 and placental growth factor: markers for identification of women destined to develop early-onset pre-eclampsia. BJOG 117(11):1384-1389
68. Ganten D, Minnich JL, Granger P, Hayduk K, Brecht HM, Barbeau A, Boucher R, Genest J (1971) Angiotensin-forming enzyme in brain tissue. Science 173(3991):64-65
69. Weinberger MH, Kramer NJ, Grim CE, Petersen LP (1977) The effect of posture and saline loading on plasma renin activity and aldosterone concentration in pregnant, non-pregnant and estrogen-treated women. J Clin Endocrinol Metab 44(1):69-77. doi:10.1210/jcem-44-1-69
70. Gordon RD, Parsons S, Symonds EM (1969) A prospective study of plasma-renin activity in normal and toxaemic pregnancy. Lancet 1(7590):347-349
71. Herse F, Dechend R, Harsem NK, Wallukat G, Janke J, Qadri F, Hering L, Muller DN, Luft FC, Staff AC (2007) Dysregulation of the circulating and tissue-based renin-angiotensin system in preeclampsia. Hypertension 49(3):604-611. doi:10.1161/01.HYP.0000257797.49289.71
72. Li C, Ansari R, Yu Z, Shah D (2000) Definitive molecular evidence of renin-angiotensin system in human uterine decidual cells. Hypertension 36(2):159-164
73. Massani ZM, Sanguinetti R, Gallegos R, Raimondi D (1967) Angiotensin blood levels in normal and toxemic pregnancies. Am J Obstet Gynecol 99(3):313-317
74. Gant NF, Daley GL, Chand S, Whalley PJ, MacDonald PC (1973) A study of angiotensin II pressor response throughout primigravid pregnancy. J Clin Invest 52(11):2682-2689. doi:10.1172/JCI107462
75. Wallukat G, Homuth V, Fischer T, Lindschau C, Horstkamp B, Jupner A, Baur E, Nissen E, Vetter K, Neichel D, Dudenhausen JW, Haller H, Luft FC (1999) Patients with preeclampsia develop agonistic autoantibodies against the angiotensin AT1 receptor. J Clin Invest 103(7):945-952. doi:10.1172/JCI4106
76. LaMarca B, Parrish M, Ray LF, Murphy SR, Roberts L, Glover P, Wallukat G, Wenzel K, Cockrell K, Martin JN Jr, Ryan MJ, Dechend R (2009) Hypertension in response to autoantibodies to the angiotensin II type I receptor (AT1-AA) in pregnant rats: role of endothelin-1. Hypertension 54(4):905-909. doi:10.1161/HYPERTENSIONAHA.109.137935
77. Zhou CC, Zhang Y, Irani RA, Zhang H, Mi T, Popek EJ, Hicks MJ, Ramin SM, Kellems RE, Xia Y (2008) Angiotensin receptor agonistic autoantibodies induce pre-eclampsia in pregnant mice. Nat Med 14(8):855-862. doi:10.1038/nm.1856
78. LaMarca B, Wallace K, Herse F, Wallukat G, Martin JN Jr, Weimer A, Dechend R (2011) Hypertension in response to placental ischemia during pregnancy: role of B lymphocytes. Hypertension 57(4):865-871. doi:10.1161/HYPERTENSIONAHA.110.167569
79. Novotny SR, Wallace K, Heath J, Moseley J, Dhillon P, Weimer A, Wallukat G, Herse F, Wenzel K, Martin JN Jr, Dechend R, Lamarca B (2012) Activating autoantibodies to the angiotensin II type I receptor play an important role in mediating hypertension in response to adoptive transfer of CD4+ T lymphocytes from placental ischemic rats. Am J Physiol Regul Integr Comp Physiol 302(10):R1197-1201. doi:10.1152/ajpregu.00623.2011
80. Parikh SM, Karumanchi SA (2008) Putting pressure on preeclampsia. Nat Med 14(8):810-812. doi:10.1038/nm0808-810
81. Dragun D, Muller DN, Brasen JH, Fritsche L, Nieminen-Kelha M, Dechend R, Kintscher U, Rudolph B, Hoebeke J, Eckert D, Mazak I, Plehm R, Schonemann C, Unger T, Budde K, Neumayer HH, Luft FC, Wallukat G (2005) Angiotensin II type 1-receptor activating antibodies in renal-allograft rejection. N Engl J Med 352(6):558-569. doi:10.1056/NEJMoa035717
82. Riemekasten G, Philippe A, Nather M, Slowinski T, Muller DN, Heidecke H, Matucci-Cerinic M, Czirjak L, Lukitsch I, Becker M, Kill A, van Laar JM, Catar R, Luft FC, Burmester GR, Hegner B, Dragun D (2011) Involvement of functional autoantibodies against vascular receptors in systemic sclerosis. Ann Rheum Dis 70(3):530-536. doi:10.1136/ard.2010.135772
83. Giral M, Foucher Y, Dufay A, Van Huyen JP, Renaudin K, Moreau A, Philippe A, Hegner B, Dechend R, Heidecke H, Brouard S, Cesbron A, Castagnet S, Devys A, Soulillou JP, Dragun D (2013) Pretransplant sensitization against angiotensin II type 1 receptor is a risk factor for acute rejection and graft loss. Am J Transplant 13(10):2567-2576. doi:10.1111/ajt.12397
84. Saxena AR, Karumanchi SA, Brown NJ, Royle CM, McElrath TF, Seely EW (2010) Increased sensitivity to angiotensin II is present postpartum in women with a history of hypertensive pregnancy. Hypertension 55(5):1239-1245. doi:10.1161/HYPERTENSIONAHA.109.147595
85. Hladunewich MA, Kingdom J, Odutayo A, Burns K, Lai V, O'Brien T, Gandhi S, Zimpelmann J, Kiss A, Miller J, Cherney D (2011) Postpartum assessment of the renin angiotensin system in women with previous severe, early-onset preeclampsia. J Clin Endocrinol Metab 96(11):3517-3524. doi:10.1210/jc.2011-1125
86. Kvehaugen AS, Melien O, Holmen OL, Laivuori H, Oian P, Andersgaard AB, Dechend R, Staff AC (2013) Single nucleotide polymorphisms in G protein signaling pathway genes in preeclampsia. Hypertension 61(3):655-661. doi:10.1161/HYPERTENSIONAHA.111.00331
87. Wenzel K, Rajakumar A, Haase H, Geusens N, Hubner N, Schulz H, Brewer J, Roberts L, Hubel CA, Herse F, Hering L, Qadri F, Lindschau C, Wallukat G, Pijnenborg R, Heidecke H, Riemekasten G, Luft FC, Muller DN, Lamarca B, Dechend R (2011) Angiotensin II type 1 receptor antibodies and increased angiotensin II sensitivity in pregnant rats. Hypertension 58(1):77-84. doi:10.1161/HYPERTENSIONAHA.111.171348
88. AbdAlla S, Lother H, el Massiery A, Quitterer U (2001) Increased AT(1) receptor heterodimers in preeclampsia mediate enhanced angiotensin II responsiveness. Nat Med 7(9):1003-1009. doi:10.1038/nm0901-1003
89. Zhou A, Carrell RW, Murphy MP, Wei Z, Yan Y, Stanley PL, Stein PE, Broughton Pipkin F, Read RJ (2010) A redox switch in angiotensinogen modulates angiotensin release. Nature 468(7320):108-111. doi:10.1038/nature09505
90. Anton L, Brosnihan KB (2008) Systemic and uteroplacental renin-angiotensin system in normal and pre-eclamptic pregnancies. Ther Adv Cardiovasc Dis 2(5):349-362. doi:10.1177/1753944708094529
91. Herse F, Staff AC, Hering L, Muller DN, Luft FC, Dechend R (2008) AT1-receptor autoantibodies and uteroplacental RAS in pregnancy and pre-eclampsia. J Mol Med (Berl) 86(6):697-703. doi:10.1007/s00109-008-0332-4
92. Hering L, Herse F, Geusens N, Verlohren S, Wenzel K, Staff AC, Brosnihan KB, Huppertz B, Luft FC, Muller DN, Pijnenborg R, Cartwright JE, Dechend R (2010) Effects of circulating and local uteroplacental angiotensin II in rat pregnancy. Hypertension 56(2):311-318. doi:10.1161/HYPERTENSIONAHA.110.150961
93. Shah DM, Banu JM, Chirgwin JM, Tekmal RR (2000) Reproductive tissue renin gene expression in preeclampsia. Hypertens Pregnancy 19(3):341-351 pii:100101996
94. Anton L, Merrill DC, Neves LA, Gruver C, Moorefield C, Brosnihan KB (2010) Angiotensin II and angiotensin-(1-7) decrease sFlt1 release in normal but not preeclamptic chorionic villi: an in vitro study. Reprod Biol Endocrinol 8:135. doi:10.1186/1477-7827-8-135
95. Mosca L, Benjamin EJ, Berra K, Bezanson JL, Dolor RJ, Lloyd-Jones DM, Newby LK, Pina IL, Roger VL, Shaw LJ, Zhao D, Beckie TM, Bushnell C, D'Armiento J, Kris-Etherton PM, Fang J, Ganiats TG, Gomes AS, Gracia CR, Haan CK, Jackson EA, Judelson DR, Kelepouris E, Lavie CJ, Moore A, Nussmeier NA, Ofili E, Oparil S, Ouyang P, Pinn VW, Sherif K, Smith SC Jr, Sopko G, Chandra-Strobos N, Urbina EM, Vaccarino V, Wenger NK (2011) Effectiveness-based guidelines for the prevention of cardiovascular disease in women - 2011 update: a guideline from the american heart association. Circulation 123(11):1243-1262. doi:10.1161/CIR.0b013e31820faaf8
96. Irgens HU, Reisaeter L, Irgens LM, Lie RT (2001) Long term mortality of mothers and fathers after pre-eclampsia: population based cohort study. BMJ 323(7323):1213-1217
97. Bellamy L, Casas JP, Hingorani AD, Williams DJ (2007) Preeclampsia and risk of cardiovascular disease and cancer in later life: systematic review and meta-analysis. BMJ 335(7627):974. doi:10.1136/bmj.39335.385301.BE
98. Lykke JA, Langhoff-Roos J, Sibai BM, Funai EF, Triche EW, Paidas MJ (2009) Hypertensive pregnancy disorders and subsequent cardiovascular morbidity and type 2 diabetes mellitus in the mother. Hypertension 53(6):944-951. doi:10.1161/HYPERTENSIONAHA.109.130765
99. Wikstrom AK, Haglund B, Olovsson M, Lindeberg SN (2005) The risk of maternal ischaemic heart disease after gestational hypertensive disease. BJOG 112(11):1486-1491. doi:10.1111/j.1471-0528.2005.00733.x
100. Harsem NK, Roald B, Braekke K, Staff AC (2007) Acute atherosis in decidual tissue: not associated with systemic oxidative stress in preeclampsia. Placenta 28(8-9):958-964. doi:10.1016/j.placenta.2006.11.005
101. Hanssens M, Pijnenborg R, Keirse MJ, Vercruysse L, Verbist L, Van Assche FA (1998) Renin-like immunoreactivity in uterus and placenta from normotensive and hypertensive pregnancies. Eur J Obstet Gynecol Reprod Biol 81(2):177-184
102. Staff AC, Dechend R, Redman CW (2013) Review: preeclampsia, acute atherosis of the spiral arteries and future cardiovascular disease: two new hypotheses. Placenta 34(Suppl):S73-78. doi:10.1016/j.placenta.2012.11.022
103. Staff AC, Redman CW (2014) IFPA Award in Placentology Lecture: preeclampsia, the decidual battleground and future maternal cardiovascular disease. Placenta 35(Suppl):S26-31. doi:10.1016/j.placenta.2013.12.003
104. Tenhola S, Rahiala E, Martikainen A, Halonen P, Voutilainen R (2003) Blood pressure, serum lipids, fasting insulin, and adrenal hormones in 12-year-old children born with maternal preeclampsia. J Clin Endocrinol Metab 88(3):1217-1222. doi:10.1210/jc.2002-020903
105. Vatten LJ, Romundstad PR, Holmen TL, Hsieh CC, Trichopoulos D, Stuver SO (2003) Intrauterine exposure to preeclampsia and adolescent blood pressure, body size, and age at menarche in female offspring. Obstet Gynecol 101(3):529-533 pii:S0029784402027187
106. Oglaend B, Forman MR, Romundstad PR, Nilsen ST, Vatten LJ (2009) Blood pressure in early adolescence in the offspring of preeclamptic and normotensive pregnancies. J Hypertens 27(10):2051-2054. doi:10.1097/HJH.0b013e328330052a
107. Ros HS, Lichtenstein P, Ekbom A, Cnattingius S (2001) Tall or short? Twenty years after preeclampsia exposure in utero: comparisons of final height, body mass index, waist-to-hip ratio, and age at menarche among women, exposed and unexposed to preeclampsia during fetal life. Pediatr Res 49(6):763-769. doi:10.1203/00006450-200106000-00008