Thrombosis Research
Volume 124, Issue 4 , Pages 393-396 , September 2009

Tissue factor and the endometrium: From physiology to pathology

Received 25 March 2009 ,Revised 11 May 2009 ,Accepted 2 June 2009.

References 

  1. Fusi L, Cloke B, Brosens JJ. The uterine junctional zone. Best Pract Res. 2006;20:479–491
  2. Salamonsen LA, Hannan NJ, Dimitriadis E. Cytokines and chemokines during human embryo implantation: roles in implantation and early placentation. Semin Reprod Med. 2007;25:437–444
  3. Lockwood CJ, Krikun G, Schatz F. The decidua regulates hemostasis in human endometrium. Semin Reprod Endocrinol. 1999;17:45–51
  4. Bach R, Nemerson Y, Konigsberg W. Purification and characterization of bovine tissue factor. J Biol Chem. 1981;256:8324–8331
  5. Kirchhofer D, Nemerson Y. Initiation of blood coagulation: the tissue factor/factor VIIa complex. Curr Opin Biotechnol. 1996;7:386–391
  6. Nemerson Y. Tissue factor and hemostasis. Blood. 1988;71:1–8
  7. Nemerson Y. Tissue factor: then and now. Thromb Haemost. 1995;74:180–184
  8. Szotowski B, Antoniak S, Rauch U. Alternatively spliced tissue factor: a previously unknown piece in the puzzle of hemostasis. Trends Cardiovasc Med. 2006;16:177–182
  9. Muller YA, Ultsch MH, Kelley RF, de Vos AM. Structure of the extracellular domain of human tissue factor: location of the factor VIIa binding site. Biochemistry. 1994;33:10864–10870
  10. Bluff JE, Brown NJ, Reed MW, Staton CA. Tissue factor, angiogenesis and tumour progression. Breast Cancer Res. 2008;10:204
  11. Bach RR. Tissue factor encryption. Arterioscler Thromb Vasc Biol. 2006;26:456–461
  12. Eilertsen KE, Osterud B. Tissue factor: (patho)physiology and cellular biology. Blood Coagul Fibrinolysis. 2004;15:521–538
  13. Price GC, Thompson SA, Kam PC. Tissue factor and tissue factor pathway inhibitor. Anaesthesia. 2004;59:483–492
  14. Nemerson Y. My life with tissue factor. J Thromb Haemost. 2007;5:221–223
  15. Guha A, Bach R, Konigsberg W, Nemerson Y. Affinity purification of human tissue factor: interaction of factor VII and tissue factor in detergent micelles. Proc Natl Acad Sci U S A. 1986;83:299–302
  16. Spicer EK, Horton R, Bloem L, Bach R, Williams KR, Guha A, et al. Isolation of cDNA clones coding for human tissue factor: primary structure of the protein and cDNA. Proc Natl Acad Sci U S A. 1987;84:5148–5152
  17. Osterud B, Rapaport SI. Activation of factor IX by the reaction product of tissue factor and factor VII: additional pathway for initiating blood coagulation. Proc Natl Acad Sci U S A. 1977;74:5260–5264
  18. Mackman N. Role of tissue factor in hemostasis and thrombosis. Blood Cells Mol Diseases. 2006;36:104–107
  19. Mackman N. Role of tissue factor in hemostasis, thrombosis, and vascular development. Arterioscler Thromb Vasc Biol. 2004;24:1015–1022
  20. Morrissey JH, Pureza V, Davis-Harrison RL, Sligar SG, Ohkubo YZ, Tajkhorshid E. Blood clotting reactions on nanoscale phospholipid bilayers. Thromb Res. 2008;122(Suppl 1):S23–S26
  21. Rao LV, Pendurthi UR. Regulation of tissue factor-factor VIIa expression on cell surfaces: a role for tissue factor-factor VIIa endocytosis. Mol Cell Biochem. 2003;253:131–140
  22. Mackman N. Regulation of the tissue factor gene. Faseb J. 1995;9:883–889
  23. Chen VM, Ahamed J, Versteeg HH, Berndt MC, Ruf W, Hogg PJ. Evidence for activation of tissue factor by an allosteric disulfide bond. Biochemistry. 2006;45:12020–12028
  24. Chen VM, Hogg PJ. Allosteric disulfide bonds in thrombosis and thrombolysis. J Thromb Haemost. 2006;4:2533–2541
  25. Wolberg AS, Monroe DM, Roberts HR, Hoffman MR. Tissue factor de-encryption: ionophore treatment induces changes in tissue factor activity by phosphatidylserine-dependent and -independent mechanisms. Blood Coagul Fibrinolysis. 1999;10:201–210
  26. Ahamed J, Versteeg HH, Kerver M, Chen VM, Mueller BM, Hogg PJ, et al. Disulfide isomerization switches tissue factor from coagulation to cell signaling. Proc Natl Acad Sci U S A. 2006;103:13932–13937
  27. Bach R, Konigsberg WH, Nemerson Y. Human tissue factor contains thioester-linked palmitate and stearate on the cytoplasmic half-cystine. Biochemistry. 1988;27:4227–4231
  28. Versteeg HH, Peppelenbosch MP, Spek CA. Tissue factor signal transduction in angiogenesis. Carcinogenesis. 2003;24:1009–1013
  29. Versteeg HH, Ruf W. Emerging insights in tissue factor-dependent signaling events. Semin Thromb Hemost. 2006;32:24–32
  30. Lopez-Pedrera C, Barbarroja N, Dorado G, Siendones E, Velasco F. Tissue factor as an effector of angiogenesis and tumor progression in hematological malignancies. Leukemia. 2006;20:1331–1340
  31. Bugge TH, Xiao Q, Kombrinck KW, Flick MJ, Holmback K, Danton MJ, et al. Fatal embryonic bleeding events in mice lacking tissue factor, the cell-associated initiator of blood coagulation. Proc Natl Acad Sci U S A. 1996;93:6258–6263
  32. Toomey JR, Kratzer KE, Lasky NM, Stanton JJ, Broze GJ. Targeted disruption of the murine tissue factor gene results in embryonic lethality. Blood. 1996;88:1583–1587
  33. Carmeliet P, Mackman N, Moons L, Luther T, Gressens P, Van Vlaenderen I, et al. Role of tissue factor in embryonic blood vessel development. Nature. 1996;383:73–75
  34. Belting M, Dorrell MI, Sandgren S, Aguilar E, Ahamed J, Dorfleutner A, et al. Regulation of angiogenesis by tissue factor cytoplasmic domain signaling. Nat Med. 2004;10:502–509
  35. George FD. Microparticles in vascular diseases. Thromb Res. 2008;122(Suppl 1):S55–S59
  36. Lechner D, Weltermann A. Circulating tissue factor-exposing microparticles. Thromb Res. 2008;122(Suppl 1):S47–S54
  37. Agouni A, Lagrue-Lak-Hal AH, Ducluzeau PH, Mostefai HA, Draunet-Busson C, Leftheriotis G, et al. Endothelial dysfunction caused by circulating microparticles from patients with metabolic syndrome. Am J Pathol. 2008;173:1210–1219
  38. Boulanger CM, Leroyer AS, Amabile N, Tedgui A. Circulating endothelial microparticles: a new marker of vascular injury. Ann Cardiol AngeÂiol. 2008;57:149–154
  39. Gonzalez-Quintero VH, Jimenez JJ, Jy W, Mauro LM, Hortman L, O'Sullivan MJ, et al. Elevated plasma endothelial microparticles in preeclampsia. Am J Obstet Gynecol. 2003;189:589–593
  40. Morel O, Toti F, Hugel B, Freyssinet JM. Cellular microparticles: a disseminated storage pool of bioactive vascular effectors. Curr Opin Hematol. 2004;11:156–164
  41. Bogdanov VY, Balasubramanian V, Hathcock J, Vele O, Lieb M, Nemerson Y. Alternatively spliced human tissue factor: a circulating, soluble, thrombogenic protein. Nat Med. 2003;9:458–462
  42. Mackman N. Alternatively spliced tissue factor - one cut too many?. Thromb Haemost. 2007;97:5–8
  43. Schatz F, Krikun G, Caze R, Rahman M, Lockwood CJ. Progestin-regulated expression of tissue factor in decidual cells: implications in endometrial hemostasis, menstruation and angiogenesis. Steroids. 2003;68:849–860
  44. Lockwood CJ, Nemerson Y, Guller S, Krikun G, Alvarez M, Hausknecht V, et al. Progestational regulation of human endometrial stromal cell tissue factor expression during decidualization. J Clin Endocrinol Metab. 1993;76:231–236
  45. Lockwood CJ, Krikun G, Hausknecht V, Wang EY, Schatz F. Decidual cell regulation of hemostasis during implantation and menstruation. Ann N Y Acad Sci. 1997;828:188–193
  46. Runic R, Schatz F, Krey L, Demopoulos R, Thung S, Wan L, et al. Alterations in endometrial stromal cell tissue factor protein and messenger ribonucleic acid expression in patients experiencing abnormal uterine bleeding while using Norplant-2 contraception. J Clin Endocrinol Metab. 1997;82:1983–1988
  47. Erlich J, Parry GC, Fearns C, Muller M, Carmeliet P, Luther T, et al. Tissue factor is required for uterine hemostasis and maintenance of the placental labyrinth during gestation. Proc Natl Acad Sci U S A. 1999;96:8138–8143
  48. Runic R, Schatz F, Wan L, Demopoulos R, Krikun G, Lockwood CJ. Effects of norplant on endometrial tissue factor expression and blood vessel structure. J Clin Endocrinol Metab. 2000;85:3853–3859
  49. Giudice LC, Kao LC. Endometriosis. Lancet. 2004;364:1789–1799
  50. Ryan IP, Taylor RN. Endometriosis and infertility: new concepts. Obstet Gynecol Surv. 1997;52:365–371
  51. Krikun G, Schatz F, Taylor H, Lockwood CJ. Endometriosis and tissue factor. Ann N Y Acad Sci. 2008;1127:101–105
  52. Krikun G, Huang ST, Schatz F, Salafia C, Stocco C, Lockwood CJ. Thrombin activation of endometrial endothelial cells: a possible role in intrauterine growth restriction. Thromb Haemost. 2007;97:245–253
  53. Di Paolo S, Volpe P, Grandaliano G, Stallone G, Schena A, Greco P, et al. Increased placental expression of tissue factor is associated with abnormal uterine and umbilical Doppler waveforms in severe preeclampsia with fetal growth restriction. J Nephrol. 2003;16:650–657

PII: S0049-3848(09)00274-6

doi: 10.1016/j.thromres.2009.06.013

Thrombosis Research
Volume 124, Issue 4 , Pages 393-396 , September 2009