Pregnancy-Specific Glycoproteins Bind Integrin αIIbβ3 and Inhibit the Platelet-Fibrinogen Interaction

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Shanley, Daniel K ^a   Kiely, Patrick A ^b   Golla, Kalyan ^c   Allen, Seamus ^c   Martin, Kenneth ^a   O'Riordan, Ronan T ^a   Ball, Melanie ^a   Aplin, John D ^d   Singer, Bernhard B ^e   Caplice, Noel ^a   Moran, Niamh ^c   Moore, Tom ^a  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY OF LIMERICK   (Ireland)

^c ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

^e UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA2 INTEGRIN; FIBRINOGEN; INTEGRIN ALPHAIIB BETA 3; PREGNANCY ASSOCIATED GLYCOPROTEIN 1; PREGNANCY ASSOCIATED GLYCOPROTEIN 23; PREGNANCY ASSOCIATED GLYCOPROTEIN 9; PREGNANCY ASSOCIATED PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CELL INTERACTION; CONTROLLED STUDY; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; THROMBOCYTE AGGREGATION INHIBITION;

ANIMALS; BLOOD PLATELETS; CELL ADHESION; FIBRINOGEN; GLYCOPROTEINS; HUMANS; MICE; PLATELET AGGREGATION; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; PREGNANCY PROTEINS; PROTEIN BINDING;

EID: 84874581607     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057491     Document Type: Article

References (56)

1. Lin TM, Galbert SP, Kiefer D, Spellacy WN, Gall S, (1974) Characterization of four human pregnancy-associated plasma proteins. Am J Obstet Gynecol 118: 223-236.
2. Towler CM, Horne CH, Jandial V, Campbell DM, MacGillivray I, (1976) Plasma levels of pregnancy-specific beta1-glycoprotein in normal pregnancy. Br J Obstet Gynaecol. 83(10): 775-9.
3. Zhou GQ, Baranov V, Zimmermann W, Grunert F, Erhard B, et al. (1997) Highly specific monoclonal antibody demonstrates that pregnancy-specific glycoprotein (PSG) is limited to syncytiotrophoblast in human early and term placenta. Placenta 18(7): 491-501.
4. Kammerer R, Zimmermann W, (2010) Coevolution of activating and inhibitory receptors within mammalian carcinoembryonic antigen families. BMC Biol 8: 12.
5. Teglund S, Zhou GQ, Hammarström S, (1995) Characterization of cDNA encoding novel pregnancy-specific glycoprotein variants.Biochem Biophys Res Commun. 211(2): 656-664.
6. McLellan AS, Zimmermann W, Moore T, (2005) Conservation of pregnancy-specific glycoprotein (PSG) N domains following independent expansions of the gene families in rodents and primates. BMC Evol Biol 5: 39.
7. Majumdar S, Bapna BC, Mapa MK, Gupta AN, Devi PK, et al. (1982) Pregnancy specific proteins: suppression of in vitro blastogenic response to mitogen by these proteins. Int J Fertil 27: 66-69.
8. Harris SJ, Anthony FW, Jones DB, Masson GM, (1984) Pregnancy-specific beta 1-glycoprotein: effect on lymphocyte proliferation in vitro. J Reprod Immunol 6: 267-270.
9. Snyder SK, Wessner DH, Wessells JL, Waterhouse RM, Wahl LM, et al. (2001) Pregnancy-specific glycoproteins function as immunomodulators by inducing secretion of IL-10, IL-6 and TGF-beta1 by human monocytes. Am J Reprod Immunol 45: 205-216.
10. Motrán CC, Díaz FL, Gruppi A, Slavin D, Chatton B, et al. (2002) Human pregnancy-specific glycoprotein 1a (PSG1a) induces alternative activation in human and mouse monocytes and suppresses the accessory cell-dependent T cell proliferation. J Leukoc Biol 72(3): 512-521.
11. Motrán CC, Diaz FL, Montes CL, Bocco JL, Gruppi A, (2003) In vivo expression of recombinant pregnancy-specific glycoprotein 1a induces alternative activation of monocytes and enhances Th2-type immune response. Eur J Immunol 33(11): 3007-3016.
12. Bebo BF Jr, Dveksler GS, (2005) Evidence that pregnancy specific glycoproteins regulate T-Cell function and inflammatory autoimmune disease during pregnancy. Curr Drug Targets Inflamm Allergy 4(2): 231-237.
13. Ha CT, Waterhouse R, Wessells J, Wu JA, Dveksler GS, (2005) Binding of pregnancy-specific glycoprotein 17 to CD9 on macrophages induces secretion of IL-10, IL-6, PGE2, and TGF-beta1. J Leukoc Biol 77: 948-957.
14. Martínez FF, Knubel CP, Sánchez MC, Cervi L, Motrán CC, (2012) Pregnancy-specific glycoprotein 1a activates dendritic cells to provide signals for Th17-, Th2-, and Treg-cell polarization. Eur J Immunol 42(6): 1573-1584.
15. Fialová L, Kohoutová B, Pelísková Z, Malbohan I, Mikulíková L, (1991) Serum levels of trophoblast-specific beta-1-globulin (SP1) and alpha-1-fetoprotein (AFP) in pregnant women with rheumatoid arthritis. Cesk Gynekol 56(3): 166-170.
16. Wu JA, Johnson BL, Chen Y, Ha CT, Dveksler GS, (2008) Murine pregnancy-specific glycoprotein 23 induces the proangiogenic factors transforming-growth factor beta 1 and vascular endothelial growth factor a in cell types involved in vascular remodeling in pregnancy. Biol Reprod 79(6): 1054-1061.
17. Ha CT, Wu JA, Irmak S, Lisboa FA, Dizon AM, et al. (2010) Human pregnancy specific beta-1-glycoprotein 1 (PSG1) has a potential role in placental vascular morphogenesis. Biol Reprod 83: 27-35.
18. Lisboa FA, Warren J, Sulkowski G, Aparicio M, David G, et al. (2011) Pregnancy-specific glycoprotein 1 induces endothelial tubulogenesis through interaction with cell surface proteoglycans. J Biol Chem 286(9): 7577-7586.
19. Jurisicova A, Antenos M, Kapasi K, Meriano J, Casper RF, (1999) Variability in the expression of trophectodermal markers beta-human chorionic gonadotrophin, human leukocyte antigen-G and pregnancy specific beta-1 glycoprotein by the human blastocyst. Hum Reprod 14(7): 1852-1858.
20. Bersinger NA, Ødegård RA, (2004) Second- and third-trimester serum levels of placental proteins in preeclampsia and small-for-gestational age pregnancies. Acta Obstet Gynecol Scand 83(1): 37-45.
21. Pihl K, Larsen T, Laursen I, Krebs L, Christiansen M, (2009) First trimester maternal serum pregnancy-specific beta-1-glycoprotein (SP1) as a marker of adverse pregnancy outcome. Prenat Diagn 29(13): 1256-1261.
22. Ha CT, Waterhouse R, Warren J, Zimmermann W, Dveksler GS, (2008) N-glycosylation is required for binding of murine pregnancy-specific glycoproteins 17 and 19 to the receptor CD9. Am J Reprod Immunol 59(3): 251-258.
23. Sulkowski GN, Warren J, Ha CT, Dveksler GS, (2011) Characterization of receptors for murine pregnancy specific glycoproteins 17 and 23. Placenta 32(8): 603-610.
24. Zhou GQ, Hammarström S, (2001) Pregnancy-specific glycoprotein (PSG) in baboon (Papio hamadryas): family size, domain structure, and prediction of a functional region in primate PSGs. Biol Reprod 64(1): 90-99.
25. Scarborough RM, Rose JW, Hsu MA, Phillips DR, Fried VA, et al. (1991) Barbourin. A GPIIb-IIIa-specific integrin antagonist from the venom of Sistrurus m. barbouri. J Biol Chem 266(15): 9359-9362.
26. Wynne F, Ball M, McLellan AS, Dockery P, Zimmermann W, et al. (2006) Mouse pregnancy-specific glycoproteins: tissue-specific expression and evidence of association with maternal vasculature. Reproduction 131: 721-732.
27. Mamanova L, Andrews RM, James KD, Sheridan EM, Ellis PD, et al. (2010) FRT-seq: amplification-free, strand-specific transcriptome sequencing. Nat Methods 7(2): 130-132.
28. Kim J, Zhao K, Jiang P, Lu Z, Wang J, et al. (2012) Transcriptome landscape of the human placenta. BMC Genomics 13: 115.
29. Aylward K, Meade G, Ahrens I, Devocelle M, Moran N (2006) A novel functional role for the highly conserved alpha-subunit KVGFFKR motif distinct from integrin alphaIIbbeta3 activation processes. J. Thromb. Haemost. 4, 1804-1812.
30. Ren Q, Ye S, Whiteheart SW (2008) The Platelet Release Reaction: Just when you thought platelet secretion was simple. Curr Opin Hematol. 15, 537-541.
31. James AH (2010) Pregnancy and thrombotic risk. Crit Care Med 38(2 Suppl): S57-63.
32. Bates SM, Greer IA, Pabinger I, Sofaer S, Hirsh J (2008) Venous thromboembolism, thrombophilia, antithrombotic therapy, and pregnancy: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines (8th Edition). Chest. 133(6 Suppl): 844S-886S.
33. Previtali E, Bucciarelli P, Passamonti SM, Martinelli I, (2011) Risk factors for venous and arterial thrombosis. Blood Transfus 9(2): 120-138.
34. Weiler-Guettler H, Aird WC, Rayburn H, Husain M, Rosenberg RD, (1996) Developmentally regulated gene expression of thrombomodulin in postimplantation mouse embryos. Development 122: 2271-2281.
35. Edstrom CS, Calhoun DA, Christensen RD, (2000) Expression of tissue factor pathway inhibitor in human fetal and placental tissues. Early Hum Dev 59: 77-84.
36. Sood R, Kalloway S, Mast AE, Hillard CJ, Weiler H, (2006) Fetomaternal cross talk in the placental vascular bed: control of coagulation by trophoblast cells. Blood 107: 3173-3180.
37. Li W, Zheng X, Gu J-M, Ferrell GL, Brady M, et al. (2005) Extraembryonic expression of EPCR is essential for embryonic viability. Blood 106(8): 2716-2722.
38. Valera MC, Parant O, Vayssiere C, Arnal JF, Payrastre B, (2010) Physiologic and pathologic changes of platelets in pregnancy. Platelets 21(8): 587-595.
39. Kazmi RS, Lwaleed BA, (2011) New anticoagulants: how to deal with treatment failure and bleeding complications Br J Clin Pharmacol. 72(4): 593-603.
40. Bonnar J, Redman CW, Denson KW, (1976) The role of coagulation and fibrinolysis in preeclampsia. Perspect Nephrol Hypertens 5 85-93: 85-93.
41. de Boer K, ten Cate JW, Sturk A, Borm JJ, Treffers PE, (1989) Enhanced thrombin generation in normal and hypertensive pregnancy. Am J Obstet Gynecol 160: 95-100.
42. Cadroy Y, Grandjean H, Pichon J, Desprats R, Berrebi A, et al. (1993) Evaluation of six markers of haemostatic system in normal pregnancy and pregnancy complicated by hypertension or pre-eclampsia. Br.J Obstet Gynaecol 100: 416-420.
43. Schjetlein R, Haugen G, Wisloff F, (1997) Markers of intravascular coagulation and fibrinolysis in preeclampsia: association with intrauterine growth retardation. Acta Obstet Gynecol Scand 76: 541-546.
44. Chaiworapongsa T, Yoshimatsu J, Espinoza J, Kim YM, Berman S, et al. (2002) Evidence of in vivo generation of thrombin in patients with small-for-gestational-age foetuses and pre-eclampsia. J Matern Fetal Neonatal Med 11: 362-367.
45. Tanjung MT, Siddik HD, Hariman H, Koh SC, (2005) Coagulation and fibrinolysis in preeclampsia and neonates. Clin Appl Thromb Hemost 11: 467-473.
46. Dusse LM, Rios DR, Pinheiro MB, Cooper AJ, Lwaleed BA, (2010) Pre-eclampsia: relationship between coagulation, fibrinolysis and inflammation. Clin Chim Acta 412(1-2): 17-21.
47. Blumenstein M, McMaster MT, Black MA, Wu S, Prakash R, et al. (2009) A proteomic approach identifies early pregnancy biomarkers for preeclampsia: novel linkages between a predisposition to preeclampsia and cardiovascular disease. Proteomics 9(11): 2929-2945.
48. Li M, Huang SJ, (2009) Innate immunity, coagulation and placenta-related adverse pregnancy outcomes. Thromb Res 124(6): 656-662.
49. Haig D, (1993) Genetic conflicts in human pregnancy. Q Rev Biol 68(4): 495-532.
50. Zimmermann W, Weiss M, Thompson JA (1989) cDNA cloning demonstrates the expression of pregnancy-specific glycoprotein genes, a subgroup of the carcinoembryonic antigen gene family, in fetal liver. Biochem Biophys Res Commun 163, 1197-1209.
51. Durocher Y, Perret S, Kamen A, (2002) High-level and high-throughput recombinant protein production by transient transfection of suspension-growing human 293-EBNA1 cells. Nucleic Acids Res 30(2): E9.
52. Mendelsohn ME, Zhu Y, O'Neill S, (1991) The 29-kDa proteins phosphorylated in thrombin-activated human platelets are forms of the estrogen receptor-related 27-kDa heat shock protein. Proc Natl Acad Sci USA 88: 11212-11216.
53. Aylward K, Meade G, Ahrens I, Devocelle M, Moran N, (2006) A novel functional role for the highly conserved alpha-subunit KVGFFKR motif distinct from integrin alphaIIbbeta3 activation processes. J Thromb Haemost 4: 1804-1812.
54. Bernard E, Parthasarathi L, Cho MK, Aylward K, Raab M, et al. (2009) Ligand switching in cell-permeable peptides: manipulation of the alpha-integrin signature motif. ACS Chem Biol 4(6): 457-471.
55. Edwards RJ, Moran N, Devocelle M, Kiernan A, Meade G, et al. (2007) Bioinformatic discovery of novel bioactive peptides. Nat Chem Biol 3: 108-112.
56. Savage B, Almus-Jacobs F, Ruggeri ZM, (1998) Specific synergy of multiple substrate-receptor interactions in platelet thrombus formation under flow. Cell 94: 657-666.