Serum and plasma determination of angiogenic and anti-angiogenic factors yield different results: The need for standardization in clinical practice

Journal of Maternal-Fetal and Neonatal Medicine

Volumn 23, Issue 8, 2010, Pages 820-827

  Oggè, Giovanna ^a   Romero, Roberto ^a,b,c   Kusanovic, Juan Pedro ^a,b   Chaiworapongsa, Tinnakorn ^a,b   Dong, Zhong ^a   Mittal, Pooja ^a,b   Vaisbuch, Edi ^a,b   Mazaki Tovi, Shali ^a,b   Gonzalez, Juan M ^a,b   Yeo, Lami ^a,b   Hassan, Sonia S ^a,b  

^a WAYNE STATE UNIVERSITY   (United States)

^b HUTZEL HOSPITAL   (United States)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

anti angiogenic state; placental growth factor; PLGF; prediction; Preeclampsia; pregnancy; Seng; SFLT 1; soluble endoglin; SVEGFR 1; SVEGFR 2; vascular endothelial growth factor

Indexed keywords

ANGIOGENIC FACTOR; ANTIANGIOGENIC FACTOR; EDETIC ACID; ENDOGLIN; PLACENTAL GROWTH FACTOR; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; CELL SURFACE RECEPTOR; ENG PROTEIN, HUMAN; LEUKOCYTE ANTIGEN; PLACENTA PROTEIN;

ADOLESCENT; ADULT; ARTICLE; BLOOD SAMPLING; BLOOD STORAGE; CENTRIFUGATION; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; PATHOGENESIS; PREECLAMPSIA; PREGNANCY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; STANDARDIZATION; TUBE; VEIN PUNCTURE; BLOOD; COMPARATIVE STUDY; CROSS-SECTIONAL STUDY; PLASMA; SERUM; STANDARD; YOUNG ADULT;

ADOLESCENT; ADULT; ANTIGENS, CD; CROSS-SECTIONAL STUDIES; FEMALE; HUMANS; PLASMA; PRE-ECLAMPSIA; PREGNANCY; PREGNANCY PROTEINS; RECEPTORS, CELL SURFACE; REFERENCE STANDARDS; SERUM; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; YOUNG ADULT;

EID: 77954716018     PISSN: 14767058     EISSN: 14764954     Source Type: Journal    
DOI: 10.3109/14767050903366119     Document Type: Article

References (85)

1. Lyall F, Greer IA, Boswell F, Fleming R. Suppression of serum vascular endothelial growth factor immunoreactivity in normal pregnancy and in pre-eclampsia. Br J Obstet Gynaecol 1997;104:223-228. Figure 1. Paired comparisons of the maternal plasma and serum concentrations of: A, sVEGFR-1; B, sVEGFR-2; C, PlGF; D, sEng in patients with preeclampsia.
2. Reuvekamp A, Velsing-Aarts FV, Poulina IE, Capello JJ, Duits AJ. Selective deficit of angiogenic growth factors characterises pregnancies complicated by pre-eclampsia. Br J Obstet Gynaecol 1999;106:1019-1022.
3. Livingston JC, Chin R, Haddad B, McKinney ET, Ahokas R, Sibai BM. Reductions of vascular endothelial growth factor and placental growth factor concentrations in severe preeclampsia. Am J Obstet Gynecol 2000;183:1554-1557.
4. Maynard SE, Min JY, Merchan J, Lim KH, Li J, Mondal S, Libermann TA, Morgan JP, Sellke FW, Stillman IE, et al. 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.
5. Torry DS, Wang HS, Wang TH, Caudle MR, Torry RJ. Preeclampsia is associated with reduced serum levels of placenta growth factor. Am J Obstet Gynecol 1998;179: 1539-1544.
6. Tidwell SC, Ho HN, Chiu WH, Torry RJ, Torry DS. Low maternal serum levels of placenta growth factor as an antecedent of clinical preeclampsia. Am J Obstet Gynecol 2001;184:1267-1272.
7. Tjoa ML, van Vugt JM, Mulders MA, Schutgens RB, Oudejans CB, van Wijk IJ. Plasma placenta growth factor levels in midtrimester pregnancies. Obstet Gynecol 2001;98: 600-607.
8. Taylor RN, Grimwood J, Taylor RS, McMaster MT, Fisher SJ, North RA. Longitudinal serum concentrations of placental growth factor: evidence for abnormal placental angiogenesis in pathologic pregnancies. Am J Obstet Gynecol 2003;188:177-182.
9. Krauss T, Pauer HU, Augustin HG. Prospective analysis of placenta growth factor (PlGF) concentrations in the plasma of women with normal pregnancy and pregnancies complicated by preeclampsia. Hypertens Pregnancy 2004;23:101-111.
10. Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, Yu KF, Schisterman EF, Thadhani R, Sachs BP, Epstein FH, et al. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 2004;350:672-683.
11. Thadhani R, Mutter WP, Wolf M, Levine RJ, Taylor RN, Sukhatme VP, Ecker J, Karumanchi SA. First trimester placental growth factor and soluble fms-like tyrosine kinase 1 and risk for preeclampsia. J Clin Endocrinol Metab 2004; 89:770-775.
12. Masuyama H, Suwaki N, Nakatsukasa H, Masumoto A, Tateishi Y, Hiramatrsu Y. Circulating angiogenic factors in preeclampsia, gestational proteinuria, and preeclampsia superimposed on chronic glomerulonephritis. Am J Obstet Gynecol 2006;194:551-556.
13. Robinson CJ, Johnson DD, Chang EY, Armstrong DM, Wang W. Evaluation of placenta growth factor and soluble Fms-like tyrosine kinase 1 receptor levels in mild and severe preeclampsia. Am J Obstet Gynecol 2006;195:255-259.
14. Moore Simas TA, Crawford SL, Solitro MJ, Frost SC, Meyer BA, Maynard SE. Angiogenic factors for the prediction of preeclampsia in high-risk women. Am J Obstet Gynecol 2007; 197:244-248.
15. Unal ER, Robinson CJ, Johnson DD, Chang EY. Secondtrimester angiogenic factors as biomarkers for future-onset preeclampsia. Am J Obstet Gynecol 2007;197:211-214.
16. Vatten LJ, Eskild A, Nilsen TI, Jeansson S, Jenum PA, Staff AC. Changes in circulating level of angiogenic factors from the first to second trimester as predictors of preeclampsia. Am J Obstet Gynecol 2007;196:239-246.
17. Lim JH, Kim SY, Park SY, Yang JH, Kim MY, Ryu HM. Effective prediction of preeclampsia by a combined ratio of angiogenesis-related factors. Obstet Gynecol 2008;111:1403-1409.
18. De Vivo A, Baviera G, Giordano D, Todarello G, Corrado F, D'anna R. Endoglin, PlGF and sFlt-1 as markers for predicting pre-eclampsia. Acta Obstet Gynecol Scand 2008; 87:837-842.
19. Teixeira PG, Cabral AC, Andrade SP, Reis ZS, da Cruz LP, Pereira JB, Martins BO, Rezende CA. Placental growth factor (PlGF) is a surrogate marker in preeclamptic hypertension. Hypertens Pregnancy 2008;27:65-73.
20. Diab AE, El-Behery MM, Ebrahiem MA, Shehata AE. Angiogenic factors for the prediction of pre-eclampsia in women with abnormal midtrimester uterine artery Doppler velocimetry. Int J Gynaecol Obstet 2008;102:146-151.
21. 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.
22. Tsatsaris V, Goffin F, Munaut C, Brichant JF, Pignon MR, Noel A, Schaaps JP, Cabrol D, Frankenne F, Foidart JM. Overexpression of the soluble vascular endothelial growth factor receptor in preeclamptic patients: pathophysiological consequences. J Clin Endocrinol Metab 2003;88:5555-5563.
23. Chaiworapongsa T, Romero R, Espinoza J, Bujold E, Mee KY, Goncalves 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;190:1541-1547.
24. McKeeman GC, Ardill JE, Caldwell CM, Hunter AJ, McClure N. Soluble vascular endothelial growth factor receptor-1 (sFlt-1) is increased throughout gestation in patients who have preeclampsia develop. Am J Obstet Gynecol 2004;191:1240-1246.
25. Bujold E, Romero R, Chaiworapongsa T, Kim YM, Kim GJ, Kim MR, Espinoza J, Goncalves LF, Edwin S, Mazor M. Evidence supporting that the excess of the sVEGFR-1 concentration in maternal plasma in preeclampsia has a uterine origin. J Matern Fetal Neonatal Med 2005;18:9-16.
26. Chaiworapongsa T, Romero R, Kim YM, Kim GJ, Kim MR, Espinoza J, Bujold E, Goncalves L, Gomez R, Edwin S, et al. Plasma soluble vascular endothelial growth factor receptor-1 concentration is elevated prior to the clinical diagnosis of preeclampsia. J Matern Fetal Neonatal Med 2005;17:3-18.
27. Shibata E, Rajakumar A, Powers RW, Larkin RW, Gilmour C, Bodnar LM, Crombleholme WR, Ness RB, Roberts JM, Hubel CA. Soluble fms-like tyrosine kinase 1 is increased in preeclampsia but not in normotensive pregnancies with smallfor-gestational-age neonates: relationship to circulating placental growth factor. J Clin Endocrinol Metab 2005;90:4895-4903.
28. Staff AC, Braekke K, Harsem NK, Lyberg T, Holthe MR. Circulating concentrations of sFlt1 (soluble fms-like tyrosine kinase 1) in fetal and maternal serum during pre-eclampsia. Eur J Obstet Gynecol Reprod Biol 2005;122:33-39.
29. Crispi F, Dominguez C, Llurba E, Martin-Gallan P, Cabero L, Gratacos E. Placental angiogenic growth factors and uterine artery Doppler findings for characterization of different subsets in preeclampsia and in isolated intrauterine growth restriction. Am J Obstet Gynecol 2006;195:201-207.
30. Wathen KA, Tuutti E, Stenman UH, Alfthan H, Halmesmaki E, Finne P, Ylikorkala O, Vuorela P. Maternal serum-soluble vascular endothelial growth factor receptor-1 in early pregnancy ending in preeclampsia or intrauterine growth retardation. J Clin Endocrinol Metab 2006;91:180-184.
31. Salahuddin S, Lee Y, Vadnais M, Sachs BP, Karumanchi SA, Lim KH. Diagnostic utility of soluble fms-like tyrosine kinase 1 and soluble endoglin in hypertensive diseases of pregnancy. Am J Obstet Gynecol 2007;197:28-126
32. Levine RJ, Lam C, Qian C, Yu KF, Maynard SE, Sachs BP, Sibai BM, Epstein FH, Romero R, Thadhani R, et al. Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl J Med 2006;355:992-1005.
33. Venkatesha S, Toporsian M, Lam C, Hanai J, Mammoto T, Kim YM, Bdolah Y, Lim KH, Yuan HT, Libermann TA, et al. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 2006;12:642-649. (Pubitemid 43865232)
34. Rana S, Karumanchi SA, Levine RJ, Venkatesha S, Rauh-Hain JA, Tamez H, Thadhani R. Sequential changes in antiangiogenic factors in early pregnancy and risk of developing preeclampsia. Hypertension 2007;50:137-142.
35. Robinson CJ, Johnson DD. Soluble endoglin as a secondtrimester marker for preeclampsia. Am J Obstet Gynecol 2007;197:174-175.
36. Staff AC, Braekke K, Johnsen GM, Karumanchi SA, Harsem NK. Circulating concentrations of soluble endoglin (CD105) in fetal and maternal serum and in amniotic fluid in preeclampsia. Am J Obstet Gynecol 2007;197:176.
37. Stepan H, Geipel A, Schwarz F, Kramer T, Wessel N, Faber R. Circulatory soluble endoglin and its predictive value for preeclampsia in second-trimester pregnancies with abnormal uterine perfusion. Am J Obstet Gynecol 2008;198:175-176.
38. Schlembach D, Beinder E. Angiogenic factors in preeclampsia. J Soc Gynecol Investig 2003;10:316A.
39. Kim SY, Park SY, Kim JW, Kim YM, Yang JH, Kim MY, Ahn H, Shin JS, Kim JO, Ryu HM. Circulating endothelial progenitor cells, plasma VEGF, VEGFR-1 and VEGFR-2 in preeclampsia. Am J Obstet Gynecol 2005;193:S74.
40. Chaiworapongsa T, Romero R, Gotsch F, Espinoza J, Nien JK, Goncalves L, Edwin S, Kim YM, Erez O, Kusanovic JP, et al. Low maternal concentrations of soluble vascular endothelial growth factor receptor-2 in preeclampsia and small for gestational age. J Matern Fetal Neonatal Med 2008;21:41-52.
41. Livingston JC, Haddad B, Gorski LA, Neblett P, Ahokas RA, Ramsey R, Sibai BM. Placenta growth factor is not an early marker for the development of severe preeclampsia. Am J Obstet Gynecol 2001;184:1218-1220.
42. Su YN, Lee CN, Cheng WF, Shau WY, Chow SN, Hsieh FJ. Decreased maternal serum placenta growth factor in early second trimester and preeclampsia. Obstet Gynecol 2001; 97:898-904.
43. Chappell LC, Seed PT, Briley A, Kelly FJ, Hunt BJ, Charnock-Jones DS, Mallet AI, Poston L. A longitudinal study of biochemical variables in women at risk of preeclampsia. Am J Obstet Gynecol 2002;187:127-136.
44. Park CW, Park JS, Shim SS, Jun JK, Yoon BH, Romero R. An elevated maternal plasma, but not amniotic fluid, soluble fms-like tyrosine kinase-1 (sFlt-1) at the time of mid-trimester genetic amniocentesis is a risk factor for preeclampsia. Am J Obstet Gynecol 2005;193:984-989.
45. Ohkuchi A, Hirashima C, Matsubara S, Suzuki H, Takahashi K, Arai F, Watanabe T, Kario K, Suzuki M. Alterations in placental growth factor levels before and after the onset of preeclampsia are more pronounced in women with early onset severe preeclampsia. Hypertens Res 2007;30:151-159.
46. Erez O, Romero R, Espinoza J, Fu W, Todem D, Kusanovic JP, Gotsch F, Edwin S, Nien JK, Chaiworapongsa T, et al. The change in concentrations of angiogenic and antiangiogenic factors in maternal plasma between the first and second trimesters in risk assessment for the subsequent development of preeclampsia and small-for-gestational age. J Matern Fetal Neonatal Med 2008;21:279-287.
47. Romero R, Nien JK, Espinoza J, Todem D, Fu W, Chung H, Kusanovic JP, Gotsh F, Erez O, Mazaki-Tovi S, et al. A longitudinal study of angiogenic (placental growth factor) and anti angiogenic (soluble endoglin and soluble VEGF 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 2008;21:9-23.
48. Polliotti BM, Fry AG, Saller DN, Mooney RA, Cox C, Miller RK. Second-trimester maternal serum placental growth factor andvascular endothelial growth factor for predictingsevere, earlyonset preeclampsia. Obstet Gynecol 2003;101:1266-1274.
49. 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.
50. Akolekar R, Zaragoza E, Poon LC, Pepes S, Nicolaides KH. Maternal serum placental growth factor at 11+0 to 13+6 weeks of gestation in the prediction of pre-eclampsia. Ultrasound Obstet Gynecol 2008;32:732-739.
51. Baumann MU, Bersinger NA, Mohaupt MG, Raio L, Gerber S, Surbek DV. First-trimester serum levels of soluble endoglin and soluble fms-like tyrosine kinase-1 as first-trimester markers for late-onset preeclampsia. Am J Obstet Gynecol 2008;199:266.
52. Than NG, Romero R, Hillermann R, Cozzi V, Nie G, Huppertz B. Prediction of preeclampsia -a workshop report. Placenta 2008;29(Suppl A):S83-S85.
53. Kusanovic JP, Romero R, Chaiworapongsa T, Erez O, Mittal P, Vaisbuch E, Mazaki-Tovi S, Gotsch F, Edwin S, Gomez R, et al. A prospective cohort study of the value of maternal plasma concentrations of angiogenic and anti-angiogenic factors in early pregnancy and midtrimester in the identification of patients destined to develop preeclampsia. J Matern Fetal Neonatal Med, in press.
54. Madazli R, Kuseyrioglu B, Uzun H, Uludag S, Ocak V. Prediction of preeclampsiawithmaternalmid-trimester placental growth factor, activin A, fibronectin and uterine artery Doppler velocimetry. Int J Gynaecol Obstet 2005;89:251-257.
55. Parra M, Rodrigo R, Barja P, Bosco C, Fernandez V, Munoz H, Soto-Chacon E. Screening test for preeclampsia through assessment of uteroplacental blood flow and biochemical markers of oxidative stress and endothelial dysfunction. Am J Obstet Gynecol 2005;193:1486-1491.
56. Yu CK, Smith GC, Papageorghiou AT, Cacho AM, Nicolaides KH. An integrated model for the prediction of preeclampsia using maternal factors and uterine artery Doppler velocimetry in unselected low-risk women. Am J Obstet Gynecol 2005;193:429-436.
57. Espinoza J, Romero R, Nien JK, Gomez R, Kusanovic JP, Goncalves LF, Medina L, Edwin S, Hassan S, Carstens M, et al. Identification of patients at risk for early onset and/or severe preeclampsia with the use of uterine artery Doppler velocimetry and placental growth factor. Am J Obstet Gynecol 2007;196:326-1313
58. Stepan H, Unversucht A, Wessel N, Faber R. Predictive value of maternal angiogenic factors in second trimester pregnancies with abnormal uterine perfusion. Hypertension 2007;49:818-824.
59. Crispi F, Llurba E, Dominguez C, Martin-Gallan P, Cabero L, Gratacos E. Predictive value of angiogenic factors and uterine artery Doppler for early-versus late-onset preeclampsia and intrauterine growth restriction. Ultrasound Obstet Gynecol 2008;31:303-309.
60. Poon LC, Kametas NA, Maiz N, Akolekar R, Nicolaides KH. First-trimester prediction of hypertensive disorders in pregnancy. Hypertension 2009;53:812-818.
61. Verheul HM, Hoekman K, Luykx-de BS, Eekman CA, Folman CC, Broxterman HJ, Pinedo HM. Platelet: transporter of vascular endothelial growth factor. Clin Cancer Res 1997;3:2187-2190.
62. Banks RE, Forbes MA, Kinsey SE, Stanley A, Ingham E, Walters C, Selby PJ. Release of the angiogenic cytokine vascular endothelial growth factor (VEGF) from platelets: significance for VEGF measurements and cancer biology. Br J Cancer 1998;77:956-964.
63. Webb NJ, Bottomley MJ, Watson CJ, Brenchley PE. Vascular endothelial growth factor (VEGF) is released from platelets during blood clotting: implications for measurement of circulating VEGF levels in clinical disease. Clin Sci (Lond) 1998;94:395-404.
64. Nielsen HJ, Werther K, Mynster T, Brunner N. Soluble vascular endothelial growth factor in various blood transfusion components. Transfusion 1999;39:1078-1083.
65. Wynendaele W, Derua R, Hoylaerts MF, Pawinski A, Waelkens E, de Bruijn EA, Paridaens R, Merlevede W, van Oosterom AT. Vascular endothelial growth factor measured in platelet poor plasma allows optimal separation between cancer patients and volunteers: a key to study an angiogenic marker in vivo? Ann Oncol 1999;10:965-971.
66. Adams J, Carder PJ, Downey S, Forbes MA, MacLennan K, Allgar V, Kaufman S, Hallam S, Bicknell R, Walker JJ, et al. Vascular endothelial growth factor (VEGF) in breast cancer: comparison of plasma, serum, and tissue VEGF and microvessel density and effects of tamoxifen. Cancer Res 2000;60: 2898-2905.
67. Jelkmann W. Pitfalls in the measurement of circulating vascular endothelial growth factor. Clin Chem 2001;47:617-623.
68. Gonzalez RP, Gomez RM, Castro RS, Nien JK, Merino PO, Etchegaray AB, Carstens MR, Medina LH, Viviani PG, Rojas IT. [A national birth weight distribution curve according to gestational age in chile from 1993 to 2000]. Rev Med Chil 2004;132:1155-1165.
69. ACOG Practice Bulletin. Diagnosis and management of preeclampsia and eclampsia. Number 33, January 2002. American College of Obstetricians and Gynecologists. Int J Gynaecol Obstet 2002;77:67-75.
70. Report of the National High Blood Pressure Education Program Working Group on high blood pressure in pregnancy. Am J Obstet Gynecol 2000;183:S1-S22.
71. Barleon B, Reusch P, Totzke F, Herzog C, Keck C, Martiny-Baron G, Marme D. Soluble VEGFR-1 secreted by endothelial cells and monocytes is present in human serum and plasma from healthy donors. Angiogenesis 2001;4:143-154.
72. Rajakumar A, Michael HM, Rajakumar PA, Shibata E, Hubel CA, Karumanchi SA, Thadhani R, Wolf M, Harger G, Markovic N. Extra-placental expression of vascular endothelial growth factor receptor-1, (Flt-1) and soluble Flt-1 (sFlt-1), by peripheral blood mononuclear cells (PBMCs) in normotensive and preeclamptic pregnant women. Placenta 2005;26:563-573.
73. 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.
74. He Y, Smith SK, Day KA, Clark DE, Licence DR, Charnock-Jones DS. Alternative splicing of vascular endothelial growth factor (VEGF)-R1 (FLT-1) pre-mRNA is important for the regulation of VEGF activity.Mol Endocrinol 1999;13:537-545.
75. Ebos JM, Bocci G, Man S, Thorpe PE, Hicklin DJ, Zhou D, Jia X, Kerbel RS. A naturally occurring soluble form of vascular endothelial growth factor receptor 2 detected in mouse and human plasma. Mol Cancer Res 2004;2:315-326.
76. Peichev M, Naiyer AJ, Pereira D, Zhu Z, Lane WJ, Williams M, Oz MC, Hicklin DJ, Witte L, Moore MA, et al. Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood 2000;95:952-958.
77. Cheifetz S, Bellon T, Cales C, Vera S, Bernabeu C, Massague 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.
78. Gougos A, St JS, Greaves A, O'Connell PJ, d'Apice AJ, Buhring HJ, Bernabeu C, van Mourik JA, Letarte M. Identification of distinct epitopes of endoglin, an RGDcontaining glycoprotein of endothelial cells, leukemic cells, and syncytiotrophoblasts. Int Immunol 1992;4:83-92.
79. Lastres P, Bellon T, Cabanas C, Sanchez-Madrid F, Acevedo A, Gougos A, Letarte M, Bernabeu C. Regulated expression on human macrophages of endoglin, an Arg-Gly-Asp-containing surface antigen. Eur J Immunol 1992;22:393-397.
80. Buhring HJ, Muller CA, Letarte M, Gougos A, Saalmuller A, van Agthoven AJ, Busch FW. Endoglin is expressed on a subpopulation of immature erythroid cells of normal human bone marrow. Leukemia 1991;5:841-847.
81. Maglione D, Guerriero V, Viglietto G, li-Bovi P, Persico MG. Isolation of a human placenta cDNA coding for a protein related to the vascular permeability factor. Proc Natl Acad Sci USA 1991;88:9267-9271.
82. Khaliq A, Li XF, Shams M, Sisi P, Acevedo CA, Whittle MJ, Weich H, Ahmed A. Localisation of placenta growth factor (PIGF) in human term placenta. Growth Factors 1996;13: 243-250.
83. Tordjman R, Delaire S, Plouet J, Ting S, Gaulard P, Fichelson S, Romeo PH, Lemarchandel V. Erythroblasts are a source of angiogenic factors. Blood 2001;97:1968-1974.
84. Autiero M, Luttun A, Tjwa M, Carmeliet P. Placental growth factor and its receptor, vascular endothelial growth factor receptor-1: novel targets for stimulation of ischemic tissue revascularization and inhibition of angiogenic and inflammatory disorders. J Thromb Haemost 2003;1:1356-1370.
85. Failla CM, Odorisio T, Cianfarani F, Schietroma C, Puddu P, Zambruno G. Placenta growth factor is induced in human keratinocytes during wound healing. J Invest Dermatol 2000; 115:388-395.