Angiogenic proteins and adipocytokines as markers for prediction of preeclampsia

Expert Review of Obstetrics and Gynecology

Volumn 5, Issue 6, 2010, Pages 717-725

  Masuyama, Hisashi ^a   Hiramatsu, Yuji ^a  

^a OKAYAMA UNIVERSITY   (Japan)

Author keywords

adipocytokine; angiogenic factor; placenta; prediction; preeclampsia

Indexed keywords

ADIPOCYTOKINE; ADIPONECTIN; ANGIOGENIC PROTEIN; ANGIOPOIETIN 1; ANGIOPOIETIN 2; ANGIOPOIETIN RECEPTOR; ENDOGLIN; PLACENTAL GROWTH FACTOR; RETINOL BINDING PROTEIN 4; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

DIAGNOSTIC VALUE; DISEASE MARKER; DOPPLER ECHOGRAPHY; HELLP SYNDROME; HUMAN; HYPERTENSION; INSULIN RESISTANCE; NONHUMAN; OBESITY; PATHOGENESIS; PATHOPHYSIOLOGY; PREDICTION; PREECLAMPSIA; PROTEIN PROTEIN INTERACTION; PROTEINURIA; REVIEW; RISK FACTOR;

EID: 78249290551     PISSN: 17474108     EISSN: None     Source Type: Journal    
DOI: 10.1586/eog.10.53     Document Type: Review

References (96)

1. Cunningham FG, Gant NF, Leveno KJ et al. Hypertensive disorders in pregnancy. In: Williams Obstetrics (21st Edition). McGraw-Hill, NY, USA, 568-573 (2001).
2. Sibai B, Dekker G, Kupferminc M. Pre-eclampsia. Lancet 365, 785-799 (2005).
3. Karumanchi SA, Maynard SE, Stillman IE et al. Preeclampsia: a renal perspective. Kidney Int. 67, 2101-2113 (2005).
4. Lain K Y, Roberts JM. Contemporary concepts of the pathogenesis and management of preeclampsia. JAMA 287, 3183-3186 (2002).
5. Duckitt K, Harrington D. Risk factors for pre-eclampsia at antenatal booking: systematic review of controlled studies. Br. Med. J. 330, 565-572 (2005).
6. Fisher SJ. The placental problem: linking abnormal cytotrophoblast differentiation to the maternal symptoms of preeclampsia. Reprod. Biol. Endocrinol. 5, 2-53 (2004).
7. Zhou Y, Damsky CH, Chiu K et al. Preeclampsia is associated with failure of human cytotrophoblasts to mimic a vascular adhesion phenotype. J. Clin. Invest. 99, 2152-2164 (1997).
8. Zhou Y, Fisher SJ, Janatpour M et al. Human cytotrophoblasts adopt a vascular phenotype as they differentiate: a strategy for successful endovascular invasion? J. Clin. Invest. 99, 2139-2151 (1997).
9. Roberts JM, Lain KY. Recent insights into the pathogenesis of preeclampsia. Placenta 23, 359-372 (2002).
10. Meekins JW, Pijnenborg R, Hanssens M et al. A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclamptic pregnancies. Br. J. Obstet. Gynaecol. 101, 669-674 (2004).
11. Huppertz B. Placental origins of preeclampsia: challenging the current hypothesis. Hypertension 51, 970-975 (2008).
12. Davison JM, Homuth V, Jeyabalan A et al. New aspects in the pathophysiology of preeclampsia. J. Am. Soc. Nephrol. 15, 2440-2448 (2004).
13. Shore VH, Wang TH, Wang CL et al. Vascular endothelial growth factor, placental growth factor and their receptors in isolated human trophoblast. Placenta 18, 657-665 (1997).
14. Polliotti BM, Fry AG, Saller DN et al. Second trimester maternal serum placental growth factor and vascular endothelial growth factor for predicting severe, early onset preeclampsia. Obstet. Gynecol. 101, 1266-1274 (2003).
15. Taylor RN, Grimwood J, Taylor RS et al. Longitudinal serum concentrations of placental growth factor: evidence for abnormal placental angiogenesis in pathogenic pregnancies. Am. J. Obstet. Gynecol. 188, 177-182 (2003).
16. Masuyama H, Suwaki N, Nakatsukasa H et al. Circulating angiogenic factors in preeclampsia, gestational proteinuria, and preeclampsia on chronic glomerulonephritis. Am. J. Obstet. Gynecol. 194, 551-556 (2006).
17. Maynard SE, Min JY, Merchan J et al. Excess placental soluble FMS-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J. Clin. Invest. 111, 649-658 (2003).
18. Koga K, Osuga Y, Yoshino O et al. Elevated serum soluble vascular endothelial growth factor receptor 1 (sVEGFR-1) levels in women with preeclampsia. J. Clin. Endocrinol. Metab. 88, 2348-2351 (2003).
19. Levine RJ, Maynard SE, Qian C et al. Circulating angiogenic factors and the risk of preeclampsia. N. Engl. J. Med. 350, 672-683 (2004).
20. Lebrin F, Deckers M, Bertolino P et al. TGF-β receptor function in the endothelium. Cardiovasc. Res. 65, 599-608 (2006).
21. Li C, Hampson IN, Hampson L et al. CD105 antagonizes the inhibitory signaling of transforming growth factor β-1 on human vascular endothelial cells. FASEB J. 14, 55-64 (2000).
22. Li C, Issa R, Kumar P et al. CD105 prevents apoptosis in hypoxic endothelial cells. J. Cell. Sci. 116, 2677-2685 (2005).
23. Jekric M, Rivas-Elena JV, Prieto M et al. Endoglin regulates nitric oxide-dependent vasodilatation. FASEB J. 18, 609-611 (2004).
24. Venkatesha S, Toporsian M, Lami C et al. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat. Med. 12, 642-649 (2006).
25. Torsian M, Gros R, Kabir MG et al. A role for endoglin in coupling eNOS activity and regulating vascular tone revealed in hereditary hemorrhagic telangiectasia. Circ. Res. 96, 684-692 (2005).
26. Levine RJ, Lam C, Qian C et al. Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N. Engl. J. Med. 355, 992-1005 (2006).
27. Masuyama H, Nakatsukasa H, Takamoto N, Hiramatsu Y. Correlation between soluble endoglin, vascular endothelial growth factor receptor-1 and adipocytokines in preeclampsia. J. Clin. Endocrinol. Metab. 92, 2672-2679 (2007).
28. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med. 1, 27-31 (1995).
29. Maeshima Y, Colorado PC, Torre A et al. Distinct antitumor properties of a type IV collagen domain derived from basement membrane. J. Biol. Chem. 275, 21340-21348 (2000).
30. Maeshima Y, Sudhakar A, Lively JC et al. Tumstatin, an endothelial cell specific inhibitor of protein synthesis. Science 295, 140-143 (2002).
31. Ferrara N. Vascular endothelial growth factor and the regulation of angiogenesis. Recent Prog. Horm. Res. 55, 15-35 (2000).
32. Dvorak HF, Brown LF, Detmar M et al. Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability and angiogenesis. Am. J. Pathol. 146, 1029-1039 (1995).
33. Suri C, Jones PF, Patan S et al. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 8 7, 1171-1180 (1996).
34. Maisonpierre PC, Suri C, Jones PF et al. Angiopoietin-2, a natural antagonist for TIE2 that disrupts in vivo angiogenesis. Science 277, 55-60 (1997).
35. Visconti R P, Richardson CD, Sato TN. Orchestration of angiogenesis and arteriovenous contribution by angiopoietins and vascular endothelial growth factor (VEGF). Proc. Natl Acad. Sci. USA 99, 8219-8224 (2002).
36. Hirokoshi K, Maeshima Y, Masuyama H et al. Increase of serum angiopoietin-2 during pregnancy is suppressed in women with preeclampsia. Am. J. Hypertens. 18, 1181-1188 (2005).
37. Hirokoshi K, Maeshima Y, Masuyama H et al. Elevated serum sFlt-1/Ang-2 ratio in women with preeclampsia. Nephron Clin. Pract. 106, 43-50 (2007).
38. Vuorela P, Matikainen MT, Kuusela P et al. Endothelial tie receptor antigen in maternal and cord blood of healthy and preeclamptic subjects. Obstet. Gynecol. 92, 179-183 (1998).
39. Gotsch F, Romero R, Kusanovic JP et al. Preeclampsia and small-for-gestational age are associated with decreased concentrations of a factor involved in angiogenesis: soluble Tie-2. J. Matern. Fetal Neonatal Med. 21, 389-402 (2008).
40. Nadar SK, Karalis I, Al Yemeni E et al. Plasma markers of angiogenesis in pregnancy induced hypertension. Thromb. Haemost. 94, 1071-1076 (2005).
41. Masuyama H, Segawa T, Sumida Y et al. Different profiles of circulating angiogenic factors and adipocytokines between earlyand late-onset pre-eclampsia. BJOG 117, 314-320 (2010).
42. Wikstrom AK, Larsson A, Eriksson UJ et al. Placental growth factor and soluble FMS-like tyrosine kinase-1 in early-onset and late-onset preeclampsia. Obstet. Gynecol. 109, 1368-1374 (2007).
43. Suwaki N, Masuyama H, Nakatsukasa H et al. Hypo-adiponectinemia and circulating angiogenic factors in overweight patients complicated with preeclampsia. Am. J. Obstet. Gynecol. 195, 1687-1692 (2006). (Pubitemid 44792620)
44. Wallukat G, Homuth V, Fischer T et al. Patients with preeclampsia develop agonistic autoantibodies against the angiotensin AT1 receptor. J. Clin. Invest. 103, 945-952 (1999).
45. Zhou CC, Ahmad S, Mi T et al. Angiotensin II induces soluble FMS-like tyrosine kinase-1 release via calcineurin signaling pathway in pregnancy. Circ. Res. 100, 88-95 (2007).
46. Zhou CC, Ahmad S, Mi T et al. Autoantibody from women with preeclampsia induces soluble FMS-like tyrosine kinase-1 production via angiotensin type I receptor and calcineurin/nuclear factor of activated T-cells signaling. Hypertension 51, 1-10 (2008).
47. Zhou CC, Zhang Y, Irani RA et al. Angiotensin receptor agonistic autoantibodies induce preeclampsia in pregnant mice. Nat. Med. 14, 855-862 (2008).
48. Xia Y, Zhou CC, Ramin SM et al. Angiotensin receptors, autoimmunity and preeclampsia. J. Immunol. 179, 3391-3395 (2007).
49. Seely EW, Solomon CG. Insulin resistance and its potential role in pregnancy-induced hypertension. J. Clin. Endocrinol. Metab. 88(6), 2393-2398 (2003).
50. Wolf M, Sandler L, Munoz K. First trimester insulin resistance and subsequent preeclampsia: a prospective study. J. Clin. Endocrinol. Metab. 87, 1563-1568 (2002).
51. Innes KE, Wimsatt JH, McDuffie R. Relative glucose tolerance and subsequent development of hypertension in pregnancy. Obstet. Gynecol. 97, 905-910 (2001).
52. Gil-Campos M, Canete RR, Gil A. Adiponectin, the missing link in insulin resistance and obesity. Clin. Nutr. 23, 963-974 (2004).
53. Fasshauer M, Paschke R. Regulation of adipocytokines and insulin resistance. Diabetologia 46, 1594-603 (2003).
54. Stefan N, Stumvoll M. Adiponectin - its role in metabolism and beyond. Horm. Metab. Res. 34, 469-474 (2002).
55. Lihn AS, Pedersen SB, Richelsen B. Adiponectin: action, regulation and association to insulin sensitivity. Obes. Rev. 6, 13-21 (2005).
56. Myers MG Jr. Leptin receptor signaling and the regulation of mammalian physiology. Recent Prog. Horm. Res. 59, 287-304 (2004).
57. Kershaw EE, Flier JS. Adipose tissue as an endocrine organ. J. Clin. Endocrinol. Metab. 89, 2548-2556 (2004).
58. Henson MC, Castracane VD. Leptin in pregnancy: an update. Biol. Reprod. 74, 218-229 (2006).
59. Suwaki N, Masuyama H, Nakatsukasa H et al. Hypo-adiponectinemia and circulating angiogenic factors in overweight patients complicated with preeclampsia. Am. J. Obstet. Gynecol. 195, 1687-1692 (2006). (Pubitemid 44792620)
60. Ramsay JE, Jamieson N, Greer IA et al. Paradoxical elevation in adiponectin concentrations in women with preeclampsia. Hypertension 42, 891-894 (2003).
61. Naruse K, Yamasaki M, Umekage H et al. Peripheral blood concentrations of adiponectin, an adipocyte specific plasma protein, in normal pregnancy and preeclampsia. J. Reprod. Immunol. 65, 65-75 (2005).
62. Seely EW, Solomon CG. Insulin resistance and its potential role in pregnancy-induced hypertension. J. Clin. Endocrinol. Metab. 88, 2393-2398 (2003).
63. Mazaki-Tovi S, Romero R, Vaisbuch E et al. Maternal serum adiponectin multimers in preeclampsia. J. Perinat. Med. 37, 349-363 (2009).
64. Ouyang Y, Chen H, Chen H. Reduced plasma adiponectin and elevated leptin in preeclampsia. Int. J. Gynaecol. Obstet. 98, 110-114 (2007).
65. Ichida K, Moriyama T, Morita H et al. Plasma adiponectin concentrations and placental adiponectin expression in pre-eclamptic women. Gynecol. Endocrinol. 23, 238-243 (2007).
66. Mise H, Sagawa N, Matsumoto T et al. Augmented placental production of leptin in preeclampsia: possible involvement of placental hypoxia. J. Clin. Endocrinol. Metab. 83, 3225-3229 (1998).
67. Anim-Nyame N, Sooranna SR, Steer PJ et al. Longitudinal analysis of maternal plasma leptin concentrations during normal pregnancy and pre-eclampsia. Hum. Reprod. 15, 2033-2036 (2000).
68. Teppa RJ, Ness RB, Crombleholme WR et al. Free leptin is increased in normal pregnancy and further increased in preeclampsia. Metabolism 49, 1043-1048 (2000).
69. Nakatsukasa H, Masuyama H, Takamoto N et al. Circulating leptin and angiogenic factors in preeclampsia patients. Endocr. J. 55, 565-573 (2008).
70. Tan KC, Xu A, Chow WS et al. Hypoadiponectinaemia is associated with impaired endothelium-dependant vasodilatation. J. Clin. Endocrinol. Metab. 89, 765-769 (2004).
71. Shimabukuro M, Higa N, Asahi T et al. Hypoadiponectinaemia is closely linked to endothelial dysfunction in man. J. Clin. Endocrinol. Metab. 88, 3236-3240 (2003).
72. Iwashima Y, Katsuya T, Ishikawa K et al. Hypoadiponectinemia is an independent risk factor for hypertension. Hypertension 43, 1318-1323 (2004).
73. D'Anna R, Baviera G, Corrado F et al. Adiponectin and insulin resistance in early-and late-onset preeclampsia. BJOG 113, 1264-1269 (2006).
74. Caminos JE, Nogueiras R, Gallego R et al. Expression and regulation of adiponectin and receptor in human and rat placenta. J. Clin. Endocrinol. Metab. 90, 4276-4286 (2005).
75. Yang Q, Graham TE, Mody N et al. Serum retinol binding protein 4 contributes to insulin resistance in obesity and Type 2 diabetes. Nature 436, 356-362 (2005).
76. Inoue S, Takamoto N, Masuyama et al. Elevated level of serum retinol-binding protein 4 in pregnancy-induced hypertension. J. Obstet. Gynaecol. Res. 35, 293-300 (2009).
77. Hladunewich M, Karumanchi SA, Lafayette R. Pathophysiology of the clinical manifestations of preeclampsia. Clin J. Am. Soc. Nephrol. 22, 543-549 (2007).
78. Kusanovic JP, Romero R, Chaiworapongsa T et al. A prospective cohort study of the value of maternal plasma concentrations of angiogenic and antiangiogenic factors in early pregnancy and midtrimester in the identification of patients destined to develop preeclampsia. J. Matern. Fetal Neonatal Med. 22, 1021-1038 (2009).
79. Romero R, Nien JK, Espinoza J et al. A longitudinal study of angiogenic (placental growth factor) and antiangiogenic (soluble endoglin and soluble vascular endothelial growth factor receptor-1) factors in normal pregnancy and patients destined to develop preeclampsia and deliver a small for gestational age neonate. J. Matern. Fetal Neonatal Med. 21, 9-23 (2008).
80. Leinonen E, Wathén KA, Alfthan H et al. Maternal serum angiopoietin-1 and-2 and Tie-2 in early pregnancy ending in preeclampsia or intrauterine growth retardation. J. Clin. Endocrinol. Metab. 95(1), 126-133 (2010).
81. Bolin M, Wiberg-Itzel E, Wikström AK et al. Angiopoietin-1/ angiopoietin-2 ratio for prediction of preeclampsia. Am. J. Hypertens. 22, 891-895 (2009).
82. Widmer M, Villar J, Benigni A et al. Mapping the theories of preeclampsia and the role of angiogenic factors. Obstet. Gynecol. 109, 168-180 (2007).
83. Levine RJ, Lindheimer MD. First trimester prediction of early preeclampsia: a possibility at last! Hypertension 53, 747-748 (2009).
84. Poon L C Y, Kametas NA, Maiz N et al. First-trimester prediction of hypertensive disorders in pregnancy. Hypertension 53, 812-818 (2009).
85. Verlohren S, Galindo A, Schlembach D et al. An automated method for the determination of the sFlt-1/PIGF ratio in the assessment of preeclampsia. Am. J. Obstet. Gynecol. 202, 161.e1-e11 (2009).
86. Oggè G, Romero R, Kusanovic JP et al. Serum and plasma determination of angiogenic and antiangiogenic factors yield different results: the need for standardization in clinical practice. J. Matern. Fetal Neonatal Med. 23(8), 820-827 (2010).
87. Fasshauer M, Waldeyer T, Seeger J. Circulating high-molecular-weight adiponectin is upregulated in preeclampsia and is related to insulin sensitivity and renal function. Eur. J. Endocrinol. 158, 197-201 (2008).
88. Chien PF, Arnott N, Gordon A et al. How useful is uterine artery Doppler flow velocimetry in the prediction of preeclampsia, intrauterine growth retardation and perinatal death? An overview. BJOG 107, 196-208 (2000).
89. Cnossen JS, Morris RK, Riet G et al. Use of uterine artery Doppler ultrasonography to predict pre-eclampsia and intrauterine growth restriction: a systematic review and bivariable meta-analysis. CMAJ 178, 701-711 (2008).
90. Barton JR, Sibai BM. Prediction and prevention of recurrent preeclampsia. Obstet. Gynecol. 112, 359-372 (2008).
91. Savvidou MD, Noori M, Anderson JM et al. Maternal endothelial function and serum concentrations of placental growth factor and soluble endoglin in women with abnormal placentation. Ultrasound Obstet. Gynecol. 32, 871-876 (2008).
92. Stepan H, Geipel A, Schwarz F et al. Circulatory soluble endoglin and its predictive value for preeclampsia in second-trimester pregnancies with abnormal uterine perfusion. Am. J. Obstet. Gynecol. 198, 175-176 (2008).
93. Stepan H, Unversucht A, Wessel N et al. Predictive value of maternal angiogenic factors in second trimester pregnancies with abnormal uterine perfusion. Hypertension 49, 818-824 (2007).
94. Crispi F, Llurba E, Domínguez C et al. Predictive value of angiogenic factors and uterine artery Doppler for early-versus lateonset pre-eclampsia and intrauterine growth restriction. Ultrasound Obstet. Gynecol. 31, 303-309 (2008).
95. Muller PR, James AH, Murtha AP et al. Circulating angiogenic factors and abnormal uterine artery Doppler velocimetry in the second trimester. Hypertens. Pregnancy 25, 183-192 (2006).
96. Savvidou MD, Yu CK, Harland LC et al. Maternal serum concentration of soluble FMS-like tyrosine kinase 1 and vascular endothelial growth factor in women with abnormal uterine artery Doppler and in those with fetal growth restriction. Am. J. Obstet. Gynecol. 195, 1668-1673 (2006).