Review: The enigmatic role of endoglin in the placenta

Placenta

Volumn 35, Issue SUPPL, 2014, Pages

  Gregory, A L ^a,b   Xu, G ^a,b,c   Sotov, V ^a,b   Letarte, M ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c FUDAN UNIVERSITY   (China)

Author keywords

BMP9; Endoglin; Endothelin 1; Preeclampsia; TGF beta; Vascular endothelium

Indexed keywords

CELL SURFACE RECEPTOR; ENG PROTEIN, HUMAN; LEUKOCYTE ANTIGEN; LIGAND;

ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; FEMALE; HUMAN; METABOLISM; PLACENTA; PREECLAMPSIA; PREGNANCY; VASCULAR ENDOTHELIUM;

ANIMALS; ANTIGENS, CD; ENDOTHELIUM, VASCULAR; FEMALE; HUMANS; LIGANDS; MOLECULAR STRUCTURE; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; RECEPTORS, CELL SURFACE;

EID: 84894354869     PISSN: 01434004     EISSN: 15323102     Source Type: Journal    
DOI: 10.1016/j.placenta.2013.10.020     Document Type: Review

References (46)

1. E.J. Quackenbush, and M. Letarte Identification of several cell surface proteins of non-T, non-B acute lymphoblastic leukemia by using monoclonal antibodies J Immunol 134 2 1985 1276 1285
2. M. Letarte, A. Greaves, and S. Vera S.F. Schlossman, L. Boumsell, W. Gilks, J. Harlan, T. Kishimoto, C. Morimoto, CD105 (endoglin) cluster report 1995 Oxford University Press Oxford 1756 1759
3. F.J. Burrows, E.J. Derbyshire, P.L. Tazzari, P. Amlot, A.F. Gazdar, and S.W. King et al. Up-regulation of endoglin on vascular endothelial cells in human solid tumors: implications for diagnosis and therapy Clin Cancer Res 1 12 1995 1623 1634
4. E. Torsney, R. Charlton, D. Parums, M. Collis, and H.M. Arthur Inducible expression of human endoglin during inflammation and wound healing in vivo Inflamm Res 51 2002 464 470
5. C. Bernabeu, J.M. Lopez-Novoa, and M. Quintanilla The emerging role of TGF-beta superfamily coreceptors in cancer Biochim Biophys Acta 1792 10 2009 954 973
6. N. Pece-Barbara, S. Vera, K. Kathirkamathamby, S. Liebner, G.M. Di Guglielmo, and E. Dejana et al. Endoglin null endothelial cells proliferate faster and are more responsive to transforming growth factor beta1 with higher affinity receptors and an activated Alk1 pathway J Biol Chem 280 30 2005 27800 27808
7. K.A. McAllister, F. Lennon, B. Bowles-Biesecker, W.C. McKinnon, E.A. Helmbold, and D.S. Markel et al. Genetic heterogeneity in hereditary haemorrhagic telangiectasia: possible correlation with clinical phenotype J Med Genet 31 1994 927 932
8. N. Pece, S. Vera, U. Cymerman, R.I. White Jr., J.L. Wrana, and M. Letarte Mutant endoglin in hereditary hemorrhagic telangiectasia type 1 is transiently expressed intracellularly and is not a dominant negative J Clin Invest 100 10 1997 2568 2579
9. M. Toporsian, R. Gros, M.G. Kabir, S. Vera, K. Govindaraju, and D.H. Eidelman et al. A role for endoglin in coupling eNOS activity and regulating vascular tone revealed in hereditary hemorrhagic telangiectasia Circ Res 96 6 2005 684 692
10. F.P. Barry, R.E. Boynton, S. Haynesworth, J.M. Murphy, and J. Zaia The monoclonal antibody SH-2, raised against human mesenchymal stem cells, recognizes an epitope on endoglin (CD105) Biochem Biophys Res Commun 265 1999 134 139
11. R.C. Perlingeiro Endoglin is required for hemangioblast and early hematopoietic development Development 134 16 2007 3041 3048
12. L. Borges, M. Iacovino, T. Mayerhofer, N. Koyano-Nakagawa, J. Baik, and D.J. Garry et al. A critical role for endoglin in the emergence of blood during embryonic development Blood 119 23 2012 5417 5428
13. P. Lastres, T. Bellon, C. Cabanas, F. Sanchez-Madrid, A. Acevedo, and A. Gougos et al. Regulated expression on human macrophages of endoglin, an Arg-Gly-Asp-containing surface antigen Eur J Immunol 22 2 1992 393 397
14. R. Qu, M.M. Silver, and M. Letarte Distribution of endoglin in early human development reveals high levels on endocardial cushion tissue mesenchyme during valve formation Cell Tissue Res 292 2 1998 333 343
15. A. Bourdeau, D.J. Dumont, and M. Letarte A murine model of hereditary hemorrhagic telangiectasia J Clin Invest 104 10 1999 1343 1351
16. S. Matsubara, A. Bourdeau, K.G. terBrugge, C. Wallace, and M. Letarte Analysis of endoglin expression in normal brain tissue and in cerebral arteriovenous malformations Stroke 31 11 2000 2653 2660
17. X. Ma, M. Labinaz, J. Goldstein, H. Miller, W.J. Keon, and M. Letarte et al. Endoglin is overexpressed after arterial injury and is required for transforming growth factor-beta-induced inhibition of smooth muscle cell migration Arterioscler Thromb Vasc Biol 20 12 2000 2546 2552
18. A. Gougos, and M. Letarte Primary structure of endoglin, an RGD-containing glycoprotein of human endothelial cells J Biol Chem 265 15 1990 8361 8364
19. A. Gougos, S. St. Jacques, A. Greaves, P.J. O'Connell, A.J.F. d'Apice, and H.-J. Buhring et al. Identification of distinct epitopes of endoglin, an RGD containing-glycoprotein of endothelial cells, leukemic cells and syncytiotrophoblasts Int Immunol 4 1 1992 83 92
20. S. St-Jacques, M. Forte, S.J. Lye, and M. Letarte Localization of endoglin, a transforming growth factor-beta binding protein, and of CD44 and integrins in placenta during the first trimester of pregnancy Biol Reprod 51 3 1994 405 413
21. I. Caniggia, C.V. Taylor, J.W.K. Ritchie, S.J. Lye, and M. Letarte Endoglin regulates trophoblast differentiation along the invasive pathway in human placental villous explants Endocrinology 138 1997 4977 4988
22. I. Caniggia, S. Grisaru-Gravnosky, M. Kuliszewsky, M. Post, and S.J. Lye Inhibition of TGF-beta 3 restores the invasive capability of extravillous trophoblasts in preeclamptic pregnancies J Clin Invest 103 12 1999 1641 1650
23. E. Rossi, F. Sanz-Rodriguez, N. Eleno, A. Duwell, F.J. Blanco, and C. Langa et al. Endothelial endoglin is involved in inflammation: role in leukocyte adhesion and transmigration Blood 121 2 2013 403 415
24. O. Llorca, A. Trujillo, F.J. Blanco, and C. Bernabeu Structural model of human endoglin, a transmembrane receptor responsible for hereditary hemorrhagic telangiectasia J Mol Biol 365 3 2007 694 705
25. A. Gougos, and M. Letarte Biochemical characterization of the 44G4 antigen from the HOON pre-B leukemic cell line J Immunol 141 6 1988 1934 1940
26. U. Raab, B. Velasco, P. Lastres, A. Letamendia, C. Cales, and C. Langa et al. Expression of normal and truncated forms of human endoglin Biochem J 339 Pt 3 1999 579 588
27. C.G. Li, P.B. Wilson, C. Bernabeu, U. Raab, J.M. Wang, and S. Kumar Immunodetection and characterization of soluble CD105-TGF-ß complexes J Immunol Methods 218 1998 85 93
28. L.J. Hawinkels, P. Kuiper, E. Wiercinska, H.W. Verspaget, Z. Liu, and E. Pardali et al. Matrix metalloproteinase-14 (MT1-MMP)-mediated endoglin shedding inhibits tumor angiogenesis Cancer Res 70 10 2010 4141 4150
29. S. Venkatesha, M. Toporsian, C. Lam, J. Hanai, T. Mammoto, and Y.M. Kim et al. Soluble endoglin contributes to the pathogenesis of preeclampsia Nat Med 12 6 2006 642 649
30. R. Castonguay, E.D. Werner, R.G. Matthews, E. Presman, A.W. Mulivor, and N. Solban et al. Soluble endoglin specifically binds bone morphogenetic proteins 9 and 10 via its orphan domain, inhibits blood vessel formation, and suppresses tumor growth J Biol Chem 286 34 2011 30034 30046
31. A. Alt, L. Miguel-Romero, J. Donderis, M. Aristorena, F.J. Blanco, and A. Round et al. Structural and functional insights into endoglin ligand recognition and binding PLoS One 7 2 2012 e29948
32. R.J. Levine, C. Lam, C. Qian, K.F. Yu, S.E. Maynard, and B.P. Sachs et al. Soluble endoglin and other circulating antiangiogenic factors in preeclampsia N Engl J Med 355 10 2006 992 1005
33. T.J. Kaitu'u-Lino, K.R. Palmer, C.L. Whitehead, E. Williams, M. Lappas, and S. Tong MMP-14 is expressed in preeclamptic placentas and mediates release of soluble endoglin Am J Pathol 180 3 2012 888 894
34. S. Cheifetz, T. Bellon, C. Cales, S. Vera, C. Bernabeu, and J. Massague et al. Endoglin is a component of the transforming growth factor-beta receptor system in human endothelial cells J Biol Chem 267 27 1992 19027 19030
35. Y.G. Chen, A. Hata, R.S. Lo, D. Wotton, Y. Shi, and N. Pavletich et al. Determinants of specificity in TGF-beta signal transduction Genes Dev 12 14 1998 2144 2152
36. N.K. Kapur, S. Wilson, A.A. Yunis, X. Qiao, E. Mackey, and V. Paruchuri et al. Reduced endoglin activity limits cardiac fibrosis and improves survival in heart failure Circulation 125 22 2012 2728 2738
37. J.N. Berg, C.J. Gallione, T.T. Stenzel, D.W. Johnson, W.P. Allen, and C.E. Schwartz et al. The activin receptor-like kinase 1 gene: genomic structure and mutations in hereditary hemorrhagic telangiectasia type 2 Am J Hum Genet 61 1 1997 60 67
38. F. Lebrin, M. Deckers, P. Bertolino, and P. Ten Dijke TGF-beta receptor function in the endothelium Cardiovasc Res 65 3 2005 599 608
39. N.P. Barbara, J.L. Wrana, and M. Letarte Endoglin is an accessory protein that interacts with the signaling receptor complex of multiple members of the transforming growth factor-beta superfamily J Biol Chem 274 2 1999 584 594
40. L. David, C. Mallet, S. Mazerbourg, J.J. Feige, and S. Bailly Identification of BMP9 and BMP10 as functional activators of the orphan activin receptor-like kinase 1 (ALK1) in endothelial cells Blood 109 5 2007 1953 1961
41. E.J. Choi, Y.H. Kim, S.W. Choe, Y.G. Tak, E.M. Garrido-Martin, and M. Chang et al. Enhanced responses to angiogenic cues underlie the pathogenesis of hereditary hemorrhagic telangiectasia 2 PLoS One 8 5 2013 e63138
42. N.Y. Lee, B. Ray, T. How, and G.C. Blobe Endoglin promotes transforming growth factor beta-mediated Smad 1/5/8 signaling and inhibits endothelial cell migration through its association with GIPC J Biol Chem 283 47 2008 32527 32533
43. M. Toporsian, M. Jerkic, Y.Q. Zhou, M.G. Kabir, L.X. Yu, and B.A. McIntyre et al. Spontaneous adult-onset pulmonary arterial hypertension attributable to increased endothelial oxidative stress in a murine model of hereditary hemorrhagic telangiectasia Arterioscler Thromb Vasc Biol 30 3 2010 509 517
44. M. Jerkic, M.G. Kabir, A. Davies, L.X. Yu, B.A. McIntyre, and N.W. Husain et al. Pulmonary hypertension in adult Alk1 heterozygous mice due to oxidative stress Cardiovasc Res 92 3 2011 375 384
45. G.P. Star, M. Giovinazzo, and D. Langleben Bone morphogenic protein-9 stimulates endothelin-1 release from human pulmonary microvascular endothelial cells: a potential mechanism for elevated ET-1 levels in pulmonary arterial hypertension Microvasc Res 80 3 2010 349 354
46. J.E. Park, D. Shao, P.D. Upton, P. Desouza, I.M. Adcock, and R.J. Davies et al. BMP-9 induced endothelial cell tubule formation and inhibition of migration involves Smad1 driven endothelin-1 production PLoS One 7 1 2012 e30075