HPA-1a alloantibodies reduce endothelial cell spreading and monolayer integrity

Molecular Immunology

Volumn 46, Issue 3, 2009, Pages 406-415

  van Gils, Janine M ^a   Stutterheim, Janine ^a   van Duijn, Trynette J ^a   Zwaginga, Jaap Jan ^a,b   Porcelijn, Leendert ^c   de Haas, Masja ^a,c   Hordijk, Peter L ^a  

^a SANQUIN RESEARCH   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c Sanquin Diagnostiek   (Netherlands)

Author keywords

Adhesion molecules; Endothelial cells; Human

Indexed keywords

ALLOANTIBODY; BETA3 INTEGRIN; HUMAN PLATELET ANTIGEN 1A; IMMUNOGLOBULIN G; UNCLASSIFIED DRUG;

ALLOIMMUNITY; ARTICLE; CELL ADHESION; CELL FUNCTION; CELL SPREADING; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; WOUND HEALING;

ANTIBODIES; ANTIGENS, CD; ANTIGENS, HUMAN PLATELET; CADHERINS; CELL ADHESION; CELL MEMBRANE PERMEABILITY; CELL MOVEMENT; ELECTRIC IMPEDANCE; ENDOTHELIAL CELLS; FEMALE; HUMANS; INTEGRIN BETA3; ISOANTIBODIES; UMBILICAL CORD; WOUND HEALING;

EID: 57749121302     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2008.10.015     Document Type: Article

References (57)

1. Antonova G.N., Snead C.M., Antonov A.S., Dimitropoulou C., Venema R.C., and Catravas J.D. Nitric oxide preconditioning regulates endothelial monolayer integrity via the heat shock protein 90-soluble guanylate cyclase pathway. Am. J. Physiol. Heart Circ. Physiol. 292 (2007) H893-H903
2. Bertrand G., Martageix C., Jallu V., Vitry F., and Kaplan C. Predictive value of sequential maternal anti-HPA-1a antibody concentrations for the severity of fetal alloimmune thrombocytopenia. J. Thromb. Haemost. 4 (2006) 628-637
3. Birukova A.A., Smurova K., Birukov K.G., Kaibuchi K., Garcia J.G., and Verin A.D. Role of Rho GTPases in thrombin-induced lung vascular endothelial cells barrier dysfunction. Microvasc. Res. 67 (2004) 64-77
4. Brooks P.C., Clark R.A., and Cheresh D.A. Requirement of vascular integrin alpha v beta 3 for angiogenesis. Science 264 (1994) 569-571
5. Chang Y.S., Munn L.L., Hillsley M.V., Dull R.O., Yuan J., Lakshminarayanan S., Gardner T.W., Jain R.K., and Tarbell J.M. Effect of vascular endothelial growth factor on cultured endothelial cell monolayer transport properties. Microvasc. Res. 59 (2000) 265-277
6. Cheresh D.A. Human endothelial cells synthesize and express an Arg-Gly-Asp-directed adhesion receptor involved in attachment to fibrinogen and von Willebrand factor. Proc. Natl. Acad. Sci. U.S.A. 84 (1987) 6471-6475
7. Conforti G., Dominguez-Jimenez C., Zanetti A., Gimbrone Jr. M.A., Cremona O., Marchisio P.C., and Dejana E. Human endothelial cells express integrin receptors on the luminal aspect of their membrane. Blood 80 (1992) 437-446
8. Corada M., Mariotti M., Thurston G., Smith K., Kunkel R., Brockhaus M., Lampugnani M.G., Martin-Padura I., Stoppacciaro A., Ruco L., McDonald D.M., Ward P.A., and Dejana E. Vascular endothelial-cadherin is an important determinant of microvascular integrity in vivo. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 9815-9820
9. Davoren A., Curtis B.R., Aster R.H., and McFarland J.G. Human platelet antigen-specific alloantibodies implicated in 1162 cases of neonatal alloimmune thrombocytopenia. Transfusion 44 (2004) 1220-1225
10. de Rooij J., Kerstens A., Danuser G., Schwartz M.A., and Waterman-Storer C.M. Integrin-dependent actomyosin contraction regulates epithelial cell scattering. J. Cell. Biol. 171 (2005) 153-164
11. Dettke M., Dreer M., Hocker P., and Panzer S. Human platelet antigen-1a antibodies induce the release of the chemokine RANTES from human platelets. Vox Sang. 81 (2001) 199-203
12. Drake C.J., Cheresh D.A., and Little C.D. An antagonist of integrin alpha v beta 3 prevents maturation of blood vessels during embryonic neovascularization. J. Cell. Sci. 108 Pt 7 (1995) 2655-2661
13. Dreyfus M., Kaplan C., Verdy E., Schlegel N., Durand-Zaleski I., and Tchernia G. Frequency of immune thrombocytopenia in newborns: a prospective study. Immune Thrombocytopenia Working Group. Blood 89 (1997) 4402-4406
14. Felding-Habermann B., and Cheresh D.A. Vitronectin and its receptors. Curr. Opin. Cell. Biol. 5 (1993) 864-868
15. Gao X., Kouklis P., Xu N., Minshall R.D., Sandoval R., Vogel S.M., and Malik A.B. Reversibility of increased microvessel permeability in response to VE-cadherin disassembly. Am. J. Physiol. Lung Cell. Mol. Physiol. 279 (2000) L1218-L1225
16. Ghevaert C., Campbell K., Stafford P., Metcalfe P., Casbard A., Smith G.A., Allen D., Ranasinghe E., Williamson L.M., and Ouwehand W.H. HPA-1a antibody potency and bioactivity do not predict severity of fetomaternal alloimmune thrombocytopenia. Transfusion 47 (2007) 1296-1305
17. Ghevaert C., Campbell K., Walton J., Smith G.A., Allen D., Williamson L.M., Ouwehand W.H., and Ranasinghe E. Management and outcome of 200 cases of fetomaternal alloimmune thrombocytopenia. Transfusion 47 (2007) 901-910
18. Glade-Bender J., McFarland J.G., Kaplan C., Porcelijn L., and Bussel J.B. Anti-HPA-3A induces severe neonatal alloimmune thrombocytopenia. J. Pediatr. 138 (2001) 862-867
19. Hadley A.G., Kumpel B.M., Leader K.A., Poole G.D., and Fraser I.D. Correlation of serological, quantitative and cell-mediated functional assays of maternal alloantibodies with the severity of haemolytic disease of the newborn. Br. J. Haematol. 77 (1991) 221-228
20. Hordijk P.L., Anthony E., Mul F.P., Rientsma R., Oomen L.C., and Roos D. Vascular-endothelial-cadherin modulates endothelial monolayer permeability. J. Cell. Sci. 112 Pt 12 (1999) 1915-1923
21. Hoshiga M., Alpers C.E., Smith L.L., Giachelli C.M., and Schwartz S.M. Alpha-v beta-3 integrin expression in normal and atherosclerotic artery. Circ. Res. 77 (1995) 1129-1135
22. Jaegtvik S., Husebekk A., Aune B., Oian P., Dahl L.B., and Skogen B. Neonatal alloimmune thrombocytopenia due to anti-HPA 1a antibodies; the level of maternal antibodies predicts the severity of thrombocytopenia in the newborn. BJOG 107 (2000) 691-694
23. Jaffe E.A., Nachman R.L., Becker C.G., and Minick C.R. Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. J. Clin. Invest 52 (1973) 2745-2756
24. Kaplan C., Morel-Kopp M.C., Kroll H., Kiefel V., Schlegel N., Chesnel N., and Mueller-Eckhardt C. HPA-5b (Br(a)) neonatal alloimmune thrombocytopenia: clinical and immunological analysis of 39 cases. Br. J. Haematol. 78 (1991) 425-429
25. Kay H.H., Hage M.L., Kurtzberg J., and Dunsmore K.P. Alloimmune thrombocytopenia may be associated with systemic disease. Am. J. Obstet. Gynecol. 166 (1992) 110-111
26. Keese C.R., Wegener J., Walker S.R., and Giaever I. Electrical wound-healing assay for cells in vitro. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 1554-1559
27. Kiefel V., Santoso S., Weisheit M., and Mueller-Eckhardt C. Monoclonal antibody-specific immobilization of platelet antigens (MAIPA): a new tool for the identification of platelet-reactive antibodies. Blood 70 (1987) 1722-1726
28. Kjeldsen-Kragh J., Killie M.K., Tomter G., Golebiowska E., Randen I., Hauge R., Aune B., Oian P., Dahl L.B., Pirhonen J., Lindeman R., Husby H., Haugen G., Gronn M., Skogen B., and Husebekk A. A screening and intervention program aimed to reduce mortality and serious morbidity associated with severe neonatal alloimmune thrombocytopenia. Blood 110 (2007) 833-839
29. Kroll H., Penke G., and Santoso S. Functional heterogeneity of alloantibodies against the human platelet antigen (HPA)-1a. Thromb. Haemost. 94 (2005) 1224-1229
30. Laposata M., Dovnarsky D.K., and Shin H.S. Thrombin-induced gap formation in confluent endothelial cell monolayers in vitro. Blood 62 (1983) 549-556
31. Leavesley D.I., Schwartz M.A., Rosenfeld M., and Cheresh D.A. Integrin beta 1- and beta 3-mediated endothelial cell migration is triggered through distinct signaling mechanisms. J. Cell. Biol. 121 (1993) 163-170
32. Leeksma O.C., Giltay J.C., Zandbergen-Spaargaren J., Modderman P.W., van Mourik J.A., and dem Borne A.E. The platelet alloantigen Zwa or PlA1 is expressed by cultured endothelial cells. Br. J. Haematol. 66 (1987) 369-373
33. Lorenowicz M.J., Fernandez-Borja M., van Stalborch A.M., van Sterkenburg M.A., Hiemstra P.S., and Hordijk P.L. Microtubule dynamics and Rac-1 signaling independently regulate barrier function in lung epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 293 (2007) L1321-L1331
34. Lorenowicz M.J., Fernandez-Borja M., Kooistra M.R., Bos J.L., and Hordijk P.L. PKA and Epac1 regulate endothelial integrity and migration through parallel and independent pathways. Eur. J. Cell. Biol. (2008)
35. Maslanka K., Guz K., and Zupanska B. Antenatal screening of unselected pregnant women for HPA-1a antigen, antibody and alloimmune thrombocytopenia. Vox Sang. 85 (2003) 326-327
36. Mueller-Eckhardt C., Kiefel V., Grubert A., Kroll H., Weisheit M., Schmidt S., Mueller-Eckhardt G., and Santoso S. 348 cases of suspected neonatal alloimmune thrombocytopenia. Lancet 1 (1989) 363-366
37. Newman P.J., Derbes R.S., and Aster R.H. The human platelet alloantigens, PlA1 and PlA2, are associated with a leucine33/proline33 amino acid polymorphism in membrane glycoprotein IIIa, and are distinguishable by DNA typing. J. Clin. Invest. 83 (1989) 1778-1781
38. Ni H., Chen P., Spring C.M., Sayeh E., Semple J.W., Lazarus A.H., Hynes R.O., and Freedman J. A novel murine model of fetal and neonatal alloimmune thrombocytopenia: response to intravenous IgG therapy. Blood 107 (2006) 2976-2983
39. Ozaki M., Ogita H., and Takai Y. Involvement of integrin-induced activation of protein kinase C in the formation of adherens junctions. Genes Cells 12 (2007) 651-662
40. Phillips D.R., Jennings L.K., and Edwards H.H. Identification of membrane proteins mediating the interaction of human platelets. J. Cell. Biol. 86 (1980) 77-86
41. Proulx C., Filion M., Goldman M., Bradley A., Devine D., Decary F., and Chartrand P. Analysis of immunoglobulin class. IgG subclass and titre of HPA-1a antibodies in alloimmunized mothers giving birth to babies with or without neonatal alloimmune thrombocytopenia. Br. J. Haematol. 87 (1994) 813-817
42. Radder C.M., Beekhuizen H., Kanhai H.H., and Brand A. Effect of maternal anti-HPA-1a antibodies and polyclonal IVIG on the activation status of vascular endothelial cells. Clin. Exp. Immunol. 137 (2004) 216-222
43. Royall J.A., Berkow R.L., Beckman J.S., Cunningham M.K., Matalon S., and Freeman B.A. Tumor necrosis factor and interleukin 1 alpha increase vascular endothelial permeability. Am. J. Physiol. 257 (1989) L399-L410
44. Sadeghi M.M., Krassilnikova S., Zhang J., Gharaei A.A., Fassaei H.R., Esmailzadeh L., Kooshkabadi A., Edwards S., Yalamanchili P., Harris T.D., Sinusas A.J., Zaret B.L., and Bender J.R. Detection of injury-induced vascular remodeling by targeting activated alphavbeta3 integrin in vivo. Circulation 110 (2004) 84-90
45. Sajid M., and Stouffer G.A. The role of alpha(v)beta3 integrins in vascular healing. Thromb. Haemost. 87 (2002) 187-193
46. Santoso S., Kroll H., Andrei-Selmer C.L., Socher I., Rankin A., Kretzschmar E., Watkins N.A., and Ouwehand W.H. A naturally occurring LeuVal mutation in beta3-integrin impairs the HPA-1a epitope: the third allele of HPA-1. Transfusion 46 (2006) 790-799
47. Senger D.R., Ledbetter S.R., Claffey K.P., Papadopoulos-Sergiou A., Peruzzi C.A., and Detmar M. Stimulation of endothelial cell migration by vascular permeability factor/vascular endothelial growth factor through cooperative mechanisms involving the alphavbeta3 integrin, osteopontin, and thrombin. Am. J. Pathol. 149 (1996) 293-305
48. Singh B., Fu C., and Bhattacharya J. Vascular expression of the alpha(v)beta(3)-integrin in lung and other organs. Am. J. Physiol. Lung Cell. Mol. Physiol. 278 (2000) L217-L226
49. Swerlick R.A., Brown E.J., Xu Y., Lee K.H., Manos S., and Lawley T.J. Expression and modulation of the vitronectin receptor on human dermal microvascular endothelial cells. J. Invest. Dermatol. 99 (1992) 715-722
50. Tetteroo P.A., Lansdorp P.M., Leeksma O.C., and dem Borne A.E. Monoclonal antibodies against human platelet glycoprotein IIIa. Br. J. Haematol. 55 (1983) 509-522
51. Thiagarajan P., Shapiro S.S., Levine E., DeMarco L., and Yalcin A. A monoclonal antibody to human platelet glycoprotein IIIa detects a related protein in cultured human endothelial cells. J. Clin. Invest. 75 (1985) 896-901
52. Tiruppathi C., Malik A.B., Del Vecchio P.J., Keese C.R., and Giaever I. Electrical method for detection of endothelial cell shape change in real time: assessment of endothelial barrier function. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 7919-7923
53. Turner M.L., Bessos H., Fagge T., Harkness M., Rentoul F., Seymour J., Wilson D., Gray I., Ahya R., Cairns J., and Urbaniak S. Prospective epidemiologic study of the outcome and cost-effectiveness of antenatal screening to detect neonatal alloimmune thrombocytopenia due to anti-HPA-1a. Transfusion 45 (2005) 1945-1956
54. Valentin N., Visentin G.P., and Newman P.J. Involvement of the cysteine-rich domain of glycoprotein IIIa in the expression of the human platelet alloantigen, PlA1: evidence for heterogeneity in the humoral response. Blood 85 (1995) 3028-3033
55. Wang Y., Jin G., Miao H., Li J.Y., Usami S., and Chien S. Integrins regulate VE-cadherin and catenins: dependence of this regulation on Src, but not on Ras. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 1774-1779
56. Wegener J., Keese C.R., and Giaever I. Electric cell-substrate impedance sensing (ECIS) as a noninvasive means to monitor the kinetics of cell spreading to artificial surfaces. Exp. Cell. Res. 259 (2000) 158-166
57. Williamson L.M., Hackett G., Rennie J., Palmer C.R., Maciver C., Hadfield R., Hughes D., Jobson S., and Ouwehand W.H. The natural history of fetomaternal alloimmunization to the platelet-specific antigen HPA-1a (PlA1, Zwa) as determined by antenatal screening. Blood 92 (1998) 2280-2287