Angiogenic factors in preeclampsia: From diagnosis to therapy

Hypertension

Volumn 67, Issue 6, 2016, Pages 1072-1079

  Karumanchi, S Ananth ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b Center for Vascular Biology Research   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENIC FACTOR; BIOLOGICAL MARKER; DEXTRAN SULFATE; ENDOGLIN; ENDOTHELIN RECEPTOR ANTAGONIST; HYDROGEN SULFIDE; LOW DENSITY LIPOPROTEIN CHOLESTEROL; NITRIC OXIDE; OUABAIN; PHOSPHOLIPID ANTIBODY; PLACENTAL GROWTH FACTOR; PREGNANCY ASSOCIATED PLASMA PROTEIN A; PROCOAGULANT; PROSTACYCLIN; RELAXIN; SILDENAFIL; TRANSFORMING GROWTH FACTOR BETA1; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1; ENG PROTEIN, HUMAN; FLT1 PROTEIN, HUMAN; PGF PROTEIN, HUMAN;

APHERESIS; ARTICLE; BLOOD VESSEL INJURY; CHRONIC KIDNEY DISEASE; DIABETES MELLITUS; DIAGNOSTIC KIT; DISEASE PREDISPOSITION; DISSEMINATED INTRAVASCULAR CLOTTING; DRUG EFFICACY; ENDOTHELIUM INJURY; HETEROLOGOUS EXPRESSION; HIGH RISK POPULATION; HUMAN; HYPERCHOLESTEROLEMIA; HYPERTENSION; INTRAUTERINE GROWTH RETARDATION; KIDNEY FAILURE; MULTIPLE PREGNANCY; NONHUMAN; OBESITY; PERIPARTUM CARDIOMYOPATHY; POSTERIOR REVERSIBLE ENCEPHALOPATHY SYNDROME; PREECLAMPSIA; PRIORITY JOURNAL; PROTEINURIA; SEIZURE; SOLUTIO PLACENTAE; SYSTEMIC LUPUS ERYTHEMATOSUS; THROMBOPHILIA; TRISOMY 13; VASCULAR REMODELING; ANIMAL; FEMALE; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MOLECULARLY TARGETED THERAPY; NEOVASCULARIZATION (PATHOLOGY); PLACENTA; PREGNANCY; PROGNOSIS; VASCULARIZATION;

ANIMALS; BIOMARKERS; ENDOGLIN; FEMALE; GENE EXPRESSION PROFILING; HUMANS; MOLECULAR TARGETED THERAPY; NEOVASCULARIZATION, PATHOLOGIC; PLACENTA; PLACENTA GROWTH FACTOR; PRE-ECLAMPSIA; PREGNANCY; PROGNOSIS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 84963706370     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.116.06421     Document Type: Article

References (109)

1. Abalos E, Cuesta C, Grosso AL, Chou D, Say L, Global and regional estimates of preeclampsia and eclampsia: a systematic review. Eur J Obstet Gynecol Reprod Biol 2013 170 1 7. doi: 10.1016/j.ejogrb.2013.05.005
2. Fisher KA, Luger A, Spargo BH, Lindheimer MD, Hypertension in pregnancy: clinical-pathological correlations and remote prognosis. Medicine (Baltimore) 1981 60 267 276
3. Spargo B, McCartney CP, Winemiller R, Glomerular capillary endotheliosis in toxemia of pregnancy. Arch Pathol 1959 68 593 599
4. Duley L, The global impact of pre-eclampsia and eclampsia. Semin Perinatol 2009 33 130 137. doi: 10.1053/j.semperi.2009.02.010
5. Powe CE, Levine RJ, Karumanchi SA, Preeclampsia, a disease of the maternal endothelium: the role of antiangiogenic factors and implications for later cardiovascular disease. Circulation 2011 123 2856 2869. doi: 10.1161/CIRCULATIONAHA.109.853127
6. Sibai BM, Ewell M, Levine RJ, Klebanoff MA, Esterlitz J, Catalano PM, Goldenberg RL, Joffe G, Risk factors associated with preeclampsia in healthy nulliparous women. The Calcium for Preeclampsia Prevention (CPEP) Study Group. Am J Obstet Gynecol 1997 177 1003 1010
7. Esplin MS, Fausett MB, Fraser A, Kerber R, Mineau G, Carrillo J, Varner MW, Paternal and maternal components of the predisposition to preeclampsia. N Engl J Med 2001 344 867 872. doi: 10.1056/NEJM200103223441201
8. Palmer SK, Moore LG, Young D, Cregger B, Berman JC, Zamudio S, Altered blood pressure course during normal pregnancy and increased preeclampsia at high altitude (3100 meters) in Colorado. Am J Obstet Gynecol 1999 180 1161 1168
9. Chen XK, Wen SW, Bottomley J, Smith GN, Leader A, Walker MC, In vitro fertilization is associated with an increased risk for preeclampsia. Hypertens Pregnancy 2009 28 1 12. doi: 10.1080/10641950802001859
10. Romero R, Chaiworapongsa T, Preeclampsia: a link between trophoblast dysregulation and an antiangiogenic state. J Clin Invest 2013 123 2775 2777. doi: 10.1172/JCI70431
11. Redman CW, Sargent IL, Latest advances in understanding preeclampsia. Science 2005 308 1592 1594. doi: 10.1126/science.1111726
12. 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, Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 2003 111 649 658. doi: 10.1172/JCI17189
13. Kendall RL, Thomas KA, Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc Natl Acad Sci U S A 1993 90 10705 10709
14. Clark DE, Smith SK, He Y, Day KA, Licence DR, Corps AN, Lammoglia R, Charnock-Jones DS, A vascular endothelial growth factor antagonist is produced by the human placenta and released into the maternal circulation. Biol Reprod 1998 59 1540 1548
15. Palmer KR, Kaitu'u-Lino TJ, Hastie R, Hannan NJ, Ye L, Binder N, Cannon P, Tuohey L, Johns TG, Shub A, Tong S, Placental-specific sFLT-1 e15a protein is increased in preeclampsia, antagonizes vascular endothelial growth factor signaling, and has antiangiogenic activity. Hypertension 2015 66 1251 1259. doi: 10.1161/HYPERTENSIONAHA.115.05883
16. Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, Yu KF, Schisterman EF, Thadhani R, Sachs BP, Epstein FH, Sibai BM, Sukhatme VP, Karumanchi SA, Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 2004 350 672 683. doi: 10.1056/NEJMoa031884
17. Chaiworapongsa T, Romero R, Espinoza J, Bujold E, Mee Kim Y, Gonçalves LF, Gomez R, Edwin S, Evidence supporting a role for blockade of the vascular endothelial growth factor system in the pathophysiology of preeclampsia. Young Investigator Award. Am J Obstet Gynecol 2004 190 1541 7; discussion 1547. doi: 10.1016/j.ajog.2004.03.043
18. Chaiworapongsa T, Romero R, Kim YM, Kim GJ, Kim MR, Espinoza J, Bujold E, Gonçalves L, Gomez R, Edwin S, Mazor M, Plasma soluble vascular endothelial growth factor receptor-1 concentration is elevated prior to the clinical diagnosis of pre-eclampsia. J Matern Fetal Neonatal Med 2005 17 3 18. doi: 10.1080/14767050400028816
19. Hertig A, Berkane N, Lefevre G, Toumi K, Marti HP, Capeau J, Uzan S, Rondeau E, Maternal serum sFlt1 concentration is an early and reliable predictive marker of preeclampsia. Clin Chem 2004 50 1702 1703. doi: 10.1373/clinchem.2004.036715
20. Koga K, Osuga Y, Yoshino O, Hirota Y, Ruimeng X, Hirata T, Takeda S, Yano T, Tsutsumi O, Taketani Y, Elevated serum soluble vascular endothelial growth factor receptor 1 (sVEGFR-1) levels in women with preeclampsia. J Clin Endocrinol Metab 2003 88 2348 2351. doi: 10.1210/jc.2002-021942
21. Polliotti BM, Fry AG, Saller DN, Mooney RA, Cox C, Miller RK, Second-Trimester maternal serum placental growth factor and vascular endothelial growth factor for predicting severe, early-onset preeclampsia. Obstet Gynecol 2003 101 1266 1274
22. Ahmad S, Ahmed A, Elevated placental soluble vascular endothelial growth factor receptor-1 inhibits angiogenesis in preeclampsia. Circ Res 2004 95 884 891. doi: 10.1161/01.RES.0000147365.86159.f5
23. Bergmann A, Ahmad S, Cudmore M, Gruber AD, Wittschen P, Lindenmaier W, Christofori G, Gross V, Gonzalves ACh, Gröne HJ, Ahmed A, Weich HA, Reduction of circulating soluble Flt-1 alleviates preeclampsia-like symptoms in a mouse model. J Cell Mol Med 2010 14 6B 1857 1867. doi: 10.1111/j.1582-4934.2009.00820.x
24. Kumasawa K, Ikawa M, Kidoya H, Hasuwa H, Saito-Fujita T, Morioka Y, Takakura N, Kimura T, Okabe M, Pravastatin induces placental growth factor (PGF) and ameliorates preeclampsia in a mouse model. Proc Natl Acad Sci U S A 2011 108 1451 1455. doi: 10.1073/pnas.1011293108
25. Lu F, Longo M, Tamayo E, Maner W, Al-Hendy A, Anderson GD, Hankins GD, Saade GR, The effect of over-expression of sFlt-1 on blood pressure and the occurrence of other manifestations of preeclampsia in unrestrained conscious pregnant mice. Am J Obstet Gynecol 2007 196 396.e1 7; discussion 396.e7. doi: 10.1016/j.ajog.2006.12.024
26. Sugimoto H, Hamano Y, Charytan D, Cosgrove D, Kieran M, Sudhakar A, Kalluri R, Neutralization of circulating vascular endothelial growth factor (VEGF) by anti-VEGF antibodies and soluble VEGF receptor 1 (sFlt-1) induces proteinuria. J Biol Chem 2003 278 12605 12608. doi: 10.1074/jbc.C300012200
27. Gilbert JS, Verzwyvelt J, Colson D, Arany M, Karumanchi SA, Granger JP, Recombinant vascular endothelial growth factor 121 infusion lowers blood pressure and improves renal function in rats with placentalischemia-induced hypertension. Hypertension 2010 55 380 385. doi: 10.1161/HYPERTENSIONAHA.109.141937
28. Li Z, Zhang Y, Ying Ma J, Kapoun AM, Shao Q, Kerr I, Lam A, O'Young G, Sannajust F, Stathis P, Schreiner G, Karumanchi SA, Protter AA, Pollitt NS, Recombinant vascular endothelial growth factor 121 attenuates hypertension and improves kidney damage in a rat model of preeclampsia. Hypertension 2007 50 686 692. doi: 10.1161/HYPERTENSIONAHA.107.092098
29. Eremina V, Sood M, Haigh J, Nagy A, Lajoie G, Ferrara N, Gerber HP, Kikkawa Y, Miner JH, Quaggin SE, Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest 2003 111 707 716. doi: 10.1172/JCI17423
30. Eremina V, Jefferson JA, Kowalewska J, Hochster H, Haas M, Weisstuch J, Richardson C, Kopp JB, Kabir MG, Backx PH, Gerber HP, Ferrara N, Barisoni L, Alpers CE, Quaggin SE, VEGF inhibition and renal thrombotic microangiopathy. N Engl J Med 2008 358 1129 1136. doi: 10.1056/NEJMoa0707330
31. Glusker P, Recht L, Lane B, Reversible posterior leukoencephalopathy syndrome and bevacizumab. N Engl J Med 2006 354 980 2; discussion 980. doi: 10.1056/NEJMc052954
32. Patel TV, Morgan JA, Demetri GD, George S, Maki RG, Quigley M, Humphreys BD, A preeclampsia-like syndrome characterized by reversible hypertension and proteinuria induced by the multitargeted kinase inhibitors sunitinib and sorafenib. J Natl Cancer Inst 2008 100 282 284. doi: 10.1093/jnci/djm311
33. Vigneau C, Lorcy N, Dolley-Hitze T, Jouan F, Arlot-Bonnemains Y, Laguerre B, Verhoest G, Goujon JM, Belaud-Rotureau MA, Rioux-Leclercq N, All anti-vascular endothelial growth factor drugs can induce 'pre-eclampsia-like syndrome': a RARe study. Nephrol Dial Transplant 2014 29 325 332. doi: 10.1093/ndt/gft465
34. Robinson ES, Khankin EV, Choueiri TK, Dhawan MS, Rogers MJ, Karumanchi SA, Humphreys BD, Suppression of the nitric oxide pathway in metastatic renal cell carcinoma patients receiving vascular endothelial growth factor-signaling inhibitors. Hypertension 2010 56 1131 1136. doi: 10.1161/HYPERTENSIONAHA.110.160481
35. Saleh L, Danser JA, van den Meiracker AH, Role of endothelin in preeclampsia and hypertension following antiangiogenesis treatment. Curr Opin Nephrol Hypertens 2016 25 94 99. doi: 10.1097/MNH.0000000000000197
36. Holwerda KM, Burke SD, Faas MM, Zsengeller Z, Stillman IE, Kang PM, van Goor H, McCurley A, Jaffe IZ, Karumanchi SA, Lely AT, Hydrogen sulfide attenuates sFlt1-induced hypertension and renal damage by upregulating vascular endothelial growth factor. J Am Soc Nephrol 2014 25 717 725. doi: 10.1681/ASN.2013030291
37. Neagoe PE, Lemieux C, Sirois MG, Vascular endothelial growth factor (VEGF)-A165-induced prostacyclin synthesis requires the activation of VEGF receptor-1 and -2 heterodimer. J Biol Chem 2005 280 9904 9912. doi: 10.1074/jbc.M412017200
38. Roberts WG, Palade GE, Increased microvascular permeability and endothelial fenestration induced by vascular endothelial growth factor. J Cell Sci 1995 108 (Pt 6) 2369 2379
39. Patten IS, Rana S, Shahul S, Cardiac angiogenic imbalance leads to peripartum cardiomyopathy. Nature 2012 485 333 338. doi: 10.1038/nature11040
40. Rajakumar A, Cerdeira AS, Rana S, Zsengeller Z, Edmunds L, Jeyabalan A, Hubel CA, Stillman IE, Parikh SM, Karumanchi SA, Transcriptionally active syncytial aggregates in the maternal circulation may contribute to circulating soluble fms-like tyrosine kinase 1 in preeclampsia. Hypertension 2012 59 256 264. doi: 10.1161/HYPERTENSIONAHA.111.182170
41. Nevo O, Soleymanlou N, Wu Y, Xu J, Kingdom J, Many A, Zamudio S, Caniggia I, Increased expression of sFlt-1 in in vivo and in vitro models of human placental hypoxia is mediated by HIF-1. Am J Physiol Regul Integr Comp Physiol 2006 291 R1085 R1093. doi: 10.1152/ajpregu.00794.2005
42. Tannetta DS, Dragovic RA, Gardiner C, Redman CW, Sargent IL, Characterisation of syncytiotrophoblast vesicles in normal pregnancy and pre-eclampsia: expression of Flt-1 and endoglin. PLoS One 2013 8 e56754. doi: 10.1371/journal.pone.0056754
43. Buurma AJ, Penning ME, Prins F, Schutte JM, Bruijn JA, Wilhelmus S, Rajakumar A, Bloemenkamp KW, Karumanchi SA, Baelde HJ, Preeclampsia is associated with the presence of transcriptionally active placental fragments in the maternal lung. Hypertension 2013 62 608 613. doi: 10.1161/HYPERTENSIONAHA.113.01505
44. Cheifetz S, Bellón T, Calés C, Vera S, Bernabeu C, Massagué J, Letarte M, Endoglin is a component of the transforming growth factor-beta receptor system in human endothelial cells. J Biol Chem 1992 267 19027 19030
45. Toporsian M, Gros R, Kabir MG, Vera S, Govindaraju K, Eidelman DH, Husain M, Letarte M, A role for endoglin in coupling eNOS activity and regulating vascular tone revealed in hereditary hemorrhagic telangiectasia. Circ Res 2005 96 684 692. doi: 10.1161/01.RES.0000159936.38601.22
46. Venkatesha S, Toporsian M, Lam C, Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 2006 12 642 649. doi: 10.1038/nm1429
47. Levine RJ, Lam C, Qian C, Yu KF, Maynard SE, Sachs BP, Sibai BM, Epstein FH, Romero R, Thadhani R, Karumanchi SA, CPEP Study Group Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl J Med 2006 355 992 1005. doi: 10.1056/NEJMoa055352
48. Noori M, Donald AE, Angelakopoulou A, Hingorani AD, Williams DJ, Prospective study of placental angiogenic factors and maternal vascular function before and after preeclampsia and gestational hypertension. Circulation 2010 122 478 487. doi: 10.1161/CIRCULATIONAHA.109.895458
49. Vaisbuch E, Whitty JE, Hassan SS, Romero R, Kusanovic JP, Cotton DB, Sorokin Y, Karumanchi SA, Circulating angiogenic and antiangiogenic factors in women with eclampsia. Am J Obstet Gynecol 2011 204 152.e1 152.e9. doi: 10.1016/j.ajog.2010.08.049
50. Bdolah Y, Elchalal U, Natanson-Yaron S, Yechiam H, Bdolah-Abram T, Greenfield C, Goldman-Wohl D, Milwidsky A, Rana S, Karumanchi SA, Yagel S, Hochner-Celnikier D, Relationship between nulliparity and preeclampsia may be explained by altered circulating soluble fms-like tyrosine kinase 1. Hypertens Pregnancy 2014 33 250 259. doi: 10.3109/10641955.2013.858745
51. Bdolah Y, Lam C, Rajakumar A, Shivalingappa V, Mutter W, Sachs BP, Lim KH, Bdolah-Abram T, Epstein FH, Karumanchi SA, Twin pregnancy and the risk of preeclampsia: bigger placenta or relative ischemia? Am J Obstet Gynecol 2008 198 428.e1 428.e6. doi: 10.1016/j.ajog.2007.10.783
52. Bdolah Y, Palomaki GE, Yaron Y, Bdolah-Abram T, Goldman M, Levine RJ, Sachs BP, Haddow JE, Karumanchi SA, Circulating angiogenic proteins in trisomy 13. Am J Obstet Gynecol 2006 194 239 245. doi: 10.1016/j.ajog.2005.06.031
53. Kanter D, Lindheimer MD, Wang E, Borromeo RG, Bousfield E, Karumanchi SA, Stillman IE, Angiogenic dysfunction in molar pregnancy. Am J Obstet Gynecol 2010 202 184.e1 184.e5. doi: 10.1016/j.ajog.2009.09.005
54. Karumanchi SA, Maynard SE, Stillman IE, Epstein FH, Sukhatme VP, Preeclampsia: a renal perspective. Kidney Int 2005 67 2101 2113. doi: 10.1111/j.1523-1755.2005.00316.x
55. Kanasaki K, Palmsten K, Sugimoto H, Ahmad S, Hamano Y, Xie L, Parry S, Augustin HG, Gattone VH, Folkman J, Strauss JF, Kalluri R, Deficiency in catechol-O-methyltransferase and 2-methoxyoestradiol is associated with pre-eclampsia. Nature 2008 453 1117 1121. doi: 10.1038/nature06951
56. Cudmore M, Ahmad S, Al-Ani B, Fujisawa T, Coxall H, Chudasama K, Devey LR, Wigmore SJ, Abbas A, Hewett PW, Ahmed A, Negative regulation of soluble Flt-1 and soluble endoglin release by heme oxygenase-1. Circulation 2007 115 1789 1797. doi: 10.1161/CIRCULATIONAHA.106.660134
57. Kopcow HD, Karumanchi SA, Angiogenic factors and natural killer (NK) cells in the pathogenesis of preeclampsia. J Reprod Immunol 2007 76 23 29. doi: 10.1016/j.jri.2007.03.018
58. Zhao H, Wong RJ, Kalish FS, Nayak NR, Stevenson DK, Effect of heme oxygenase-1 deficiency on placental development. Placenta 2009 30 861 868. doi: 10.1016/j.placenta.2009.07.012
59. Zhou CC, Zhang Y, Irani RA, Zhang H, Mi T, Popek EJ, Hicks MJ, Ramin SM, Kellems RE, Xia Y, Angiotensin receptor agonistic autoantibodies induce pre-eclampsia in pregnant mice. Nat Med 2008 14 855 862. doi: 10.1038/nm.1856
60. Cui Y, Wang W, Dong N, Role of corin in trophoblast invasion and uterine spiral artery remodelling in pregnancy. Nature 2012 484 246 250. doi: 10.1038/nature10897
61. Sandgren JA, Scroggins SM, Santillan DA, Devor EJ, Gibson-Corley KN, Pierce GL, Sigmund CD, Santillan MK, Grobe JL, Vasopressin: the missing link for preeclampsia? Am J Physiol Regul Integr Comp Physiol 2015 309 R1062 R1064. doi: 10.1152/ajpregu.00073.2015
62. Burwick RM, Fichorova RN, Dawood HY, Yamamoto HS, Feinberg BB, Urinary excretion of C5b-9 in severe preeclampsia: tipping the balance of complement activation in pregnancy. Hypertension 2013 62 1040 1045. doi: 10.1161/HYPERTENSIONAHA.113.01420
63. Levine RJ, Thadhani R, Qian C, Lam C, Lim KH, Yu KF, Blink AL, Sachs BP, Epstein FH, Sibai BM, Sukhatme VP, Karumanchi SA, Urinary placental growth factor and risk of preeclampsia. JAMA 2005 293 77 85. doi: 10.1001/jama.293.1.77
64. Benton SJ, Hu Y, Xie F, Kupfer K, Lee SW, Magee LA, von Dadelszen P, Angiogenic factors as diagnostic tests for preeclampsia: a performance comparison between two commercial immunoassays. Am J Obstet Gynecol 2011 205 469.e1 469.e8. doi: 10.1016/j.ajog.2011.06.058
65. Sunderji S, Gaziano E, Wothe D, Rogers LC, Sibai B, Karumanchi SA, Hodges-Savola C, Automated assays for sVEGF R1 and PlGF as an aid in the diagnosis of preterm preeclampsia: a prospective clinical study. Am J Obstet Gynecol 2010 202 40.e1 40.e7. doi: 10.1016/j.ajog.2009.07.025
66. Verlohren S, Galindo A, Schlembach D, Zeisler H, Herraiz I, Moertl MG, Pape J, Dudenhausen JW, Denk B, Stepan H, An automated method for the determination of the sFlt-1/PIGF ratio in the assessment of preeclampsia. Am J Obstet Gynecol 2010 202 161.e1 161.e11. doi: 10.1016/j.ajog.2009.09.016
67. Rolfo A, Attini R, Nuzzo AM, Piazzese A, Parisi S, Ferraresi M, Todros T, Piccoli GB, Chronic kidney disease may be differentially diagnosed from preeclampsia by serum biomarkers. Kidney Int 2013 83 177 181. doi: 10.1038/ki.2012.348
68. Verdonk K, Visser W, Russcher H, Danser AH, Steegers EA, van den Meiracker AH, Differential diagnosis of preeclampsia: remember the soluble fms-like tyrosine kinase 1/placental growth factor ratio. Hypertension 2012 60 884 890. doi: 10.1161/HYPERTENSIONAHA.112.201459
69. Verlohren S, Herraiz I, Lapaire O, Schlembach D, Moertl M, Zeisler H, Calda P, Holzgreve W, Galindo A, Engels T, Denk B, Stepan H, The sFlt-1/PlGF ratio in different types of hypertensive pregnancy disorders and its prognostic potential in preeclamptic patients. Am J Obstet Gynecol 2012 206 58.e1 58.e8. doi: 10.1016/j.ajog.2011.07.037
70. Young B, Levine RJ, Salahuddin S, Qian C, Lim KH, Karumanchi SA, Rana S, The use of angiogenic biomarkers to differentiate non-HELLP related thrombocytopenia from HELLP syndrome. J Matern Fetal Neonatal Med 2010 23 366 370. doi: 10.1080/14767050903184207
71. Perni U, Sison C, Sharma V, Helseth G, Hawfield A, Suthanthiran M, August P, Angiogenic factors in superimposed preeclampsia: a longitudinal study of women with chronic hypertension during pregnancy. Hypertension 2012 59 740 746. doi: 10.1161/HYPERTENSIONAHA.111.181735
72. Chaiworapongsa T, Romero R, Korzeniewski SJ, Kusanovic JP, Soto E, Lam J, Dong Z, Than NG, Yeo L, Hernandez-Andrade E, Conde-Agudelo A, Hassan SS, Maternal plasma concentrations of angiogenic/antiangiogenic factors in the third trimester of pregnancy to identify the patient at risk for stillbirth at or near term and severe late preeclampsia. Am J Obstet Gynecol 2013 208 287.e1 287.e15. doi: 10.1016/j.ajog.2013.01.016
73. Herraiz I, Dröge LA, Gómez-Montes E, Henrich W, Galindo A, Verlohren S, Characterization of the soluble fms-like tyrosine kinase-1 to placental growth factor ratio in pregnancies complicated by fetal growth restriction. Obstet Gynecol 2014 124 2 Pt 1 265 273. doi: 10.1097/AOG.0000000000000367
74. Rana S, Powe CE, Salahuddin S, Verlohren S, Perschel FH, Levine RJ, Lim KH, Wenger JB, Thadhani R, Karumanchi SA, Angiogenic factors and the risk of adverse outcomes in women with suspected preeclampsia. Circulation 2012 125 911 919. doi: 10.1161/CIRCULATIONAHA.111.054361
75. Chaiworapongsa T, Romero R, Korzeniewski SJ, Cortez JM, Pappas A, Tarca AL, Chaemsaithong P, Dong Z, Yeo L, Hassan SS, Plasma concentrations of angiogenic/anti-Angiogenic factors have prognostic value in women presenting with suspected preeclampsia to the obstetrical triage area: a prospective study. J Matern Fetal Neonatal Med 2014 27 132 144. doi: 10.3109/14767058.2013.806905
76. Moore AG, Young H, Keller JM, Ojo LR, Yan J, Simas TA, Maynard SE, Angiogenic biomarkers for prediction of maternal and neonatal complications in suspected preeclampsia. J Matern Fetal Neonatal Med 2012 25 2651 2657. doi: 10.3109/14767058.2012.713055
77. Chappell LC, Duckworth S, Seed PT, Griffin M, Myers J, Mackillop L, Simpson N, Waugh J, Anumba D, Kenny LC, Redman CW, Shennan AH, Diagnostic accuracy of placental growth factor in women with suspected preeclampsia: a prospective multicenter study. Circulation 2013 128 2121 2131. doi: 10.1161/CIRCULATIONAHA.113.003215
78. Rana S, Schnettler WT, Powe C, Wenger J, Salahuddin S, Cerdeira AS, Verlohren S, Perschel FH, Arany Z, Lim KH, Thadhani R, Karumanchi SA, Clinical characterization and outcomes of preeclampsia with normal angiogenic profile. Hypertens Pregnancy 2013 32 189 201. doi: 10.3109/10641955.2013.784788
79. Zeisler H, Llurba E, Chantraine F, Vatish M, Staff AC, Sennström M, Olovsson M, Brennecke SP, Stepan H, Allegranza D, Dilba P, Schoedl M, Hund M, Verlohren S, Predictive value of the sFlt-1:PlGF ratio in women with suspected preeclampsia. N Engl J Med 2016 374 13 22. doi: 10.1056/NEJMoa1414838
80. Hagmann H, Thadhani R, Benzing T, Karumanchi SA, Stepan H, The promise of angiogenic markers for the early diagnosis and prediction of preeclampsia. Clin Chem 2012 58 837 845. doi: 10.1373/clinchem.2011.169094
81. Poon LC, Kametas NA, Maiz N, Akolekar R, Nicolaides KH, First-Trimester prediction of hypertensive disorders in pregnancy. Hypertension 2009 53 812 818. doi: 10.1161/HYPERTENSIONAHA.108.127977
82. Levine RJ, Lindheimer MD, First-Trimester prediction of early preeclampsia: a possibility at last! Hypertension 2009 53 747 748. doi: 10.1161/HYPERTENSIONAHA.109.129379
83. O'Gorman N, Wright D, Syngelaki A, Akolekar R, Wright A, Poon LC, Nicolaides KH, Competing risks model in screening for preeclampsia by maternal factors and biomarkers at 11-13 weeks gestation. Am J Obstet Gynecol 2016 214 103.e1 103.e12. doi: 10.1016/j.ajog.2015.08.034
84. Kim MY, Buyon JP, Guerra MM, Angiogenic factor imbalance early in pregnancy predicts adverse outcomes in patients with lupus and antiphospholipid antibodies: results of the PROMISSE study. Am J Obstet Gynecol 2016 214 108.e1 108.e14. doi: 10.1016/j.ajog.2015.09.066
85. Thadhani R, Kisner T, Hagmann H, Pilot study of extracorporeal removal of soluble fms-like tyrosine kinase 1 in preeclampsia. Circulation 2011 124 940 950. doi: 10.1161/CIRCULATIONAHA.111.034793
86. Thadhani R, Hagmann H, Schaarschmidt W, Removal of soluble Fms-like tyrosine kinase-1 by dextran sulfate apheresis in preeclampsia. J Am Soc Nephrol 2016 27 903 913. doi: 10.1681/ASN.2015020157
87. Costantine MM, Cleary K, Hebert MF, Ahmed MS, Brown LM, Ren Z, Easterling TR, Haas DM, Haneline LS, Caritis SN, Venkataramanan R, West H, D'Alton M, Hankins G, Eunice Kennedy Shriver National Institute of Child Health and Human Development Obstetric-Fetal Pharmacology Research Units N. Safety and pharmacokinetics of pravastatin used for the prevention of preeclampsia in high-risk pregnant women: a pilot randomized controlled trial. Am J Obstet Gynecol 2015 S0002 9378 02586-7
88. Wu FT, Stefanini MO, Mac Gabhann F, Popel AS, A compartment model of VEGF distribution in humans in the presence of soluble VEGF receptor-1 acting as a ligand trap. PLoS One 2009 4 e5108. doi: 10.1371/journal.pone.0005108
89. Suzuki H, Ohkuchi A, Matsubara S, Takei Y, Murakami M, Shibuya M, Suzuki M, Sato Y, Effect of recombinant placental growth factor 2 on hypertension induced by full-length mouse soluble fms-like tyrosine kinase 1 adenoviral vector in pregnant mice. Hypertension 2009 54 1129 1135. doi: 10.1161/HYPERTENSIONAHA.109.134668
90. Spradley FT, Tan AY, Joo WS, Daniels G, Kussie P, Karumanchi SA, Granger JP, Placental growth factor administration abolishes placental ischemia-induced hypertension. Hypertension 2016 67 740 747. doi: 10.1161/HYPERTENSIONAHA.115.06783
91. McGuane JT, Danielson LA, Debrah JE, Rubin JP, Novak J, Conrad KP, Angiogenic growth factors are new and essential players in the sustained relaxin vasodilatory pathway in rodents and humans. Hypertension 2011 57 1151 1160. doi: 10.1161/HYPERTENSIONAHA.110.165027
92. Unemori E, Sibai B, Teichman SL, Scientific rationale and design of a phase I safety study of relaxin in women with severe preeclampsia. Ann N Y Acad Sci 2009 1160 381 384. doi: 10.1111/j.1749-6632.2009.03838.x
93. Ahmed A, New insights into the etiology of preeclampsia: identification of key elusive factors for the vascular complications. Thromb Res 2011 127(suppl 3) S72 S75. doi: 10.1016/S0049-3848(11)70020-2
94. Costantine MM, Cleary K, Eunice Kennedy Shriver National Institute of Child Health and Human Development Obstetric-Fetal Pharmacology Research Units Network Pravastatin for the prevention of preeclampsia in high-risk pregnant women. Obstet Gynecol 2013 121 2 pt 1 349 353. doi: http://10.1097/AOG.0b013e31827d8ad5
95. Rana S, Rajakumar A, Geahchan C, Salahuddin S, Cerdeira AS, Burke SD, George EM, Granger JP, Karumanchi SA, Ouabain inhibits placental sFlt1 production by repressing HSP27-dependent HIF-1α pathway. FASEB J 2014 28 4324 4334. doi: 10.1096/fj.14-252684
96. Sasser JM, Murphy SR, Granger JP, Emerging drugs for preeclampsia-The endothelium as a target. Expert Opin Emerg Drugs 2015 20 527 530. doi: 10.1517/14728214.2015.1062875
97. Bellamy L, Casas JP, Hingorani AD, Williams DJ, Pre-eclampsia and risk of cardiovascular disease and cancer in later life: systematic review and meta-Analysis. BMJ 2007 335 974. doi: 10.1136/bmj.39335.385301.BE
98. Irgens HU, Reisaeter L, Irgens LM, Lie RT, Long term mortality of mothers and fathers after pre-eclampsia: population based cohort study. BMJ 2001 323 1213 1217
99. Ray JG, Vermeulen MJ, Schull MJ, Redelmeier DA, Cardiovascular health after maternal placental syndromes (CHAMPS): population-based retrospective cohort study. Lancet 2005 366 1797 1803. doi: 10.1016/S0140-6736(05)67726-4
100. Vikse BE, Irgens LM, Leivestad T, Skjaerven R, Iversen BM, Preeclampsia and the risk of end-stage renal disease. N Engl J Med 2008 359 800 809. doi: 10.1056/NEJMoa0706790
101. Mosca L, Benjamin EJ, Berra K, American Heart Association Effectiveness-based guidelines for the prevention of cardiovascular disease in women-2011 update: a guideline from the American Heart Association. J Am Coll Cardiol 2011 57 1404 1423. doi: 10.1016/j.jacc.2011.02.005
102. Romundstad PR, Magnussen EB, Smith GD, Vatten LJ, Hypertension in pregnancy and later cardiovascular risk: common antecedents? Circulation 2010 122 579 584. doi: 10.1161/CIRCULATIONAHA.110.943407
103. Epstein FH, Late vascular effects of toxemia of pregnancy. N Engl J Med 1964 271 391 395. doi: 10.1056/NEJM196408202710803
104. Rich-Edwards JW, McElrath TF, Karumanchi SA, Seely EW, Breathing life into the lifecourse approach: pregnancy history and cardiovascular disease in women. Hypertension 2010 56 331 334. doi: 10.1161/HYPERTENSIONAHA.110.156810
105. Vikse BE, Irgens LM, Karumanchi SA, Thadhani R, Reisæter AV, Skjærven R, Familial factors in the association between preeclampsia and later ESRD. Clin J Am Soc Nephrol 2012 7 1819 1826. doi: 10.2215/CJN.01820212
106. Pruthi D, Khankin EV, Blanton RM, Aronovitz M, Burke SD, McCurley A, Karumanchi SA, Jaffe IZ, Exposure to experimental preeclampsia in mice enhances the vascular response to future injury. Hypertension 2015 65 863 870. doi: 10.1161/HYPERTENSIONAHA.114.04971
107. Bytautiene E, Bulayeva N, Bhat G, Li L, Rosenblatt KP, Saade GR, Long-Term alterations in maternal plasma proteome after sFlt1-induced preeclampsia in mice. Am J Obstet Gynecol 2013 208 388.e1 388.e10. doi: 10.1016/j.ajog.2013.01.042
108. Chen CW, Jaffe IZ, Karumanchi SA, Pre-eclampsia and cardiovascular disease. Cardiovasc Res 2014 101 579 586. doi: 10.1093/cvr/cvu018
109. Hod T, Cerdeira AS, Karumanchi SA, Molecular mechanisms of preeclampsia. Cold Spring Harb Perspect Med 2015 5. doi: 10.1101/cshperspect.a023473