Translational Research
Volume 152, Issue 4 , Pages 165-177 , October 2008

Phosphatidylserine-positive erythrocytes bind to immobilized and soluble thrombospondin-1 via its heparin-binding domain

  • Suhita Gayen Betal
    • ,
  • B.N. Yamaja Setty

      Affiliations

    • Corresponding Author InformationReprint requests: B. N. Yamaja Setty, PhD, Department of Pediatrics, Thomas Jefferson University, Medical College Building, Suite #727, 1025 Walnut Street, Philadelphia, Pa 19107

Received 23 March 2008 ,Revised 22 July 2008 ,Accepted 26 July 2008.

References 

  1. Kuypers FA. Phospholipid asymmetry in health and disease. Curr Opin Hematol. 1998;5:122–131
  2. Zwaal RFA, Schroit AJ. Pathophysiologic implications of membrane phospholipid asymmetry in blood cells. Blood. 1997;89:1121–1132
  3. Wu Y, Tibrewal N, Birge RB. Phosphatidylserine recognition by phagocytes: a view to a kill. Trends Cell Biol. 2006;16:189–197
  4. Setty BNY, Kulkarni S, Stuart MJ. Role of erythrocyte phosphatidylserine in sickle red cell-endothelial adhesion. Blood. 2002;99:1564–1571
  5. Eda S, Sherman IW. Cytoadherence of malaria-infected red blood cells involves exposure of phosphatidylserine. Cell Physiol Biochem. 2002;12:373–384
  6. Bonomini M, Sirolli V, Gizzi F, Di Stante S, Grilli A, Felaco M. Enhanced adherence of human uremic erythrocytes to vascular endothelium: role of phosphatidylserine exposure. Kidney Intl. 2002;62:1358–1363
  7. Hebbel RP, Boogaerts MA, Eaton JW, Steinberg MH. Erythrocyte adherence to endothelium in sickle-cell anemia (A possible determinant of disease severity). N Engl J Med. 1980;302:992–995
  8. Manodori AB, Barabino GA, Lubin BH, Kuypers FA. Adherence of phosphatidylserine-exposing erythrocytes to endothelial matrix thrombospondin. Blood. 2000;95:1293–1300
  9. Bornstein P. Diversity of function is inherent in matricellular proteins: an appraisal of thrombospondin 1. J Cell Biol. 1995;130:503–506
  10. Chen H, Herndon ME, Lawler J. The cell biology of thrombospondin-1. Matrix Biol. 2000;19:597–614
  11. Adams JC. Thrombospondins: multifunctional regulators of cell interactions. Ann Rev Cell Dev Biol. 2001;17:25–51
  12. Elzie CA, Murphy-Ullrich JE. The N-terminus of thrombospondin: the domain stands apart. Int J Biochem Cell Biol. 2004;36:1090–1101
  13. Frazier WA. Thrombospondins. Curr Opin Cell Biol. 1991;3:792–799
  14. McPherson J, Sage H, Bornstein P. Isolation and characterization of a glycoprotein secreted by aortic endothelial cells in culture: apparent identity with platelet thrombospondin. J Biol Chem. 1981;256:11330–11336
  15. Mosher DF, Doyle MJ, Jaffe EA. Synthesis and secretion of thrombospondin by cultured human endothelial cells. J Cell Biol. 1982;93:343–348
  16. Jaffe EA, Ruggiero JT, Leung LL, Doyle MJ, McKeown-Longo PJ, Mosher DF. Cultured human fibroblasts synthesize and secrete thrombospondin and incorporate it into extracellular matrix. Proc Natl Acad Sci U S A. 1983;80:998–1002
  17. Manodori AB, Matsui NM, Chen JY, Embury SH. Enhanced adherence of sickle erythrocytes to thrombin-treated endothelial cells involves interendothelial cell gap formation. Blood. 1998;92:3445–3454
  18. Gupta K, Gupta P, Solovey A, Hebbel RP. Mechanism of interaction of thrombospondin with human endothelium and inhibition of sickle erythrocyte adhesion to human endothelial cells by heparin. Biochim Biophys Acta. 1999;1453:63–73
  19. Dixit VM, Galvin NJ, O'Rourke KM, Frazier WA. Monoclonal antibodies that recognize calcium-dependent structures of human thrombospondin: characterization and mapping of their epitopes. J Biol Chem. 1986;261:1962–1968
  20. Dixit VM, Haverstick DM, O'Rourke KM, et al. A monoclonal antibody against human thrombospondin inhibits platelet aggregation. Proc Natl Acad Sci U S A. 1985;82:3472–3476
  21. Kosfeld MD, Pavlopoulos TV, Frazier WA. Cell attachment activity of the carboxyl-terminal domain of human thrombospondin expressed in Escherichia coli. J Biol Chem. 1991;266:24257–24259
  22. Merle B, Malaval L, Lawler J, Delmas P, Clezardin P. Decorin inhibits cell attachment to thrombospondin-1 by binding to a KKTR-dependent cell adhesive site present within the N-terminal domain of thrombospondin-1. J Cellular Biochem. 1997;67:75–83
  23. Clezardin P, Lawler J, Amiral J, Quentin G, Delmas P. Identification of cell adhesive active sites in the N-terminal domain of thrombospondin-1. Biochem J. 1997;321:819–827
  24. Kuypers FA, Lewis RA, Hua M, et al. Detection of altered membrane phospholipid asymmetry in subpopulations of human red blood cells using fluorescently labeled annexin V. Blood. 1996;87:1179–1187
  25. Setty BNY, Gayen Betal S. Microvascular endothelial cells express a phosphatidylserine receptor: a functionally active receptor for phosphatidylserine-positive erythrocytes. Blood. 2008;111:905–914
  26. Setty BNY, Rao AK, Stuart MJ. Thrombophilia in sickle cell disease: the red cell connection. Blood. 2001;98:3228–3233
  27. Setty BNY, Kulkarni S, Dampier CD, Stuart MJ. Fetal hemoglobin in sickle cell anemia: relationship to erythrocyte adhesion markers and adhesion. Blood. 2001;97:2568–2573
  28. Hillery CA, Du MC, Montgomery RR, Scott JP. Increased adhesion of erythrocytes to components of the extracellular matrix: isolation and characterization of a red blood cell lipid that binds thrombospondin and laminin. Blood. 1996;87:4879–4886
  29. Raynal P, Pollard HB. Annexins: the problem of assessing the biological role for a gene family of multifunctional calcium- and phospholipid-binding proteins. Biochim Biophys Acta. 1994;1197:63–93
  30. Matsui NM, Varki A, Embury SH. Heparin inhibits the flow adhesion of sickle red blood cells to P-selectin. Blood. 2002;100:3790–3796
  31. Barabino GA, Liu XD, Ewenstein BM, Kaul DK. Anionic polysaccharides inhibit adhesion of sickle erythrocytes to the vascular endothelium and result in improved hemodynamic behavior. Blood. 1999;93:1422–1429
  32. Sugihara K, Sugihara T, Mohandas N, Hebbel RP. Thrombospondin mediates adherence of CD36+ sickle reticulocytes to endothelial cells. Blood. 1992;80:2634–2642
  33. Joneckis CC, Ackley RL, Orringer EP, Wayner EA, Parise LV. Integrin alpha 4 beta 1 and glycoprotein IV (CD36) are expressed on circulating reticulocytes in sickle cell anemia. Blood. 1993;82:3548–3555
  34. Swerlick RA, Eckman JR, Kumar A, Jeitler M, Wick TM. Alpha 4 beta 1-integrin expression on sickle reticulocytes: vascular cell adhesion molecule-1-dependent binding to endothelium. Blood. 1993;82:1891–1899
  35. Brittain JE, Milnar KJ, Anderson CS, Orringer EP, Parise LV. Integrin-associated protein is an adhesion receptor on sickle red blood cells for immobilized thrombospondin. Blood. 2001;97:2159–2164
  36. Brittain JE, Milnar KJ, Anderson CS, Orringer EP, Parise LV. Activation of sickle red blood cell adhesion via integrin-associated protein/CD47-induced signal transduction. J Clin Invest. 2001;107:1555–1562
  37. Zen Q, Cottman M, Truskey G, Fraser R, Telen MJ. Critical factors in basal cell adhesion molecule/Lutheran-mediated adhesion to laminin. J Biol Chem. 1999;274:728–734
  38. Udani M, Zen Q, Cottman M, et al. Basal cell adhesion molecule/Lutheran protein (The receptor critical for sickle cell adhesion to laminin). J Clin Invest. 1998;101:2550–2558
  39. Ugarova T, Agbanyo FR, Plow EF. Conformational changes in adhesive proteins modulate their adhesive function. Thromb Haem. 1995;74:253–257
  40. Lawler J, Simons ER. Cooperative binding of calcium to thrombospondin: the effect of calcium on the circular dichroism and limited tryptic digestion of thrombospondin. J Biol Chem. 1983;258:12098–12101
  41. Slane JMK, Mosher DF, Lai CS. Conformational change in thrombospondin induced by removal of bound Ca2+: a spin label approach. FEBS Lett. 1988;229:363–366
  42. Speziale MV, Detwiler TC. Free Thiols of platelet thrombospondin: evidence for disulfide isomerization. J Biol Chem. 1990;265:17859–17867
  43. Araiso T, Kawada S-I, Yoshida K, Hasebe K, Koyama T. Effects of Ca2+ and Mg2+ on dynamics of the polar head group of phosphatidylserine bilayers. Jpn J Physiol. 1995;45:369–380
  44. Joneckis CC, Shock DD, Cunningham ML, Orringer EP, Parise LV. Glycoprotein IV-independent adhesion of sickle red blood cells to immobilized thrombospondin under flow conditions. Blood. 1996;87:4862–4870
  45. Wun T, Paglieroni T, Tablin F, Welborn J, Nelson K, Cheung A. Platelet activation and platelet-erythrocyte aggregation in patients with sickle cell anemia. J Lab Clin Med. 1997;129:507–516
  46. Wun T, Paglieroni T, Field CL. Platelet-erythrocyte adhesion in sickle cell disease. J Investig Med. 1999;47:121–127
  47. Hofstra TC, Karla VK, Meiselman HJ, Coates TD. Sickle erythrocytes adhere to polymorphonuclear neutrophils and activate the neutrophil respiratory burst. Blood. 1996;87:4440–4447
  48. Adams JC, Lawler J. Cell-type specific adhesive interactions of skeletal myoblasts with thrombospondin-1. Mol Biol Cell. 1994;5:423–437
  49. Hirsh J, Raschke R, Warkentin TE, Dalen JE, Deykin D, Poller L. Heparin: mechanism of action, pharmacokinetics, dosing considerations, monitoring, efficacy, and safety. Chest. 1995;108:258S–275S
  50. Hirsh J, Warkentin TE, Shaughnessy SG, et al. Heparin and low-molecular-weight heparin: mechanisms of action, pharmacokinetics, dosing, monitoring, efficacy, and safety. Chest. 2001;119:64S–94S
  51. Ger-Jan CM, Sanderink G-JCM, Guimart CG, Ozoux M-L. Pharmacokinetics and pharmacodynamics of the prophylactic dose of enoxaparin once daily over 4 days in patients with renal impairment. Thrombosis Res. 2002;105:225–231
  52. Chaplin H, Monroe MC, Malecek AC, Morgan LK, Michael J, Murphy WA. Preliminary trial of minidose heparin prophylaxis for painful sickle cell crises. East Afri Med J. 1989;66:574–584

 Supported by grants U54 HL70585 and R01 HL73944 from the National Heart, Lung and Blood Institute, National Institutes of Health, Bethesda, Md.

PII: S1931-5244(08)00206-5

doi: 10.1016/j.trsl.2008.07.007

Translational Research
Volume 152, Issue 4 , Pages 165-177 , October 2008

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