Structure-function analyses of thrombomodulin by gene-targeting in mice: The cytoplasmic domain is not required for normal fetal development

Blood

Volumn 93, Issue 10, 1999, Pages 3442-3450

  Conway, Edward M ^a   Pollefeyt, Saskia ^b   Cornelissen, Jan ^b   DeBaere, Inky ^b   Steiner Mosonyi, Marta ^b   Weitz, Jeffrey I ^b   Weiler Guettler, Hartmut ^b   Carmeliet, Peter ^b   Collen, Désiré ^b  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 2 ANTIPLASMIN; PLASMINOGEN; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN C; THROMBOMODULIN;

ANIMAL TISSUE; ARTICLE; BLOOD LEVEL; FETUS DEVELOPMENT; GENE INACTIVATION; GENE TARGETING; HEMOSTASIS; MOUSE; NONHUMAN; PLASMA; PRIORITY JOURNAL; PROTEIN DOMAIN; STRUCTURE ANALYSIS;

EID: 0033562859     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood.v93.10.3442.410k17_3442_3450     Document Type: Article

References (49)

1. Boffa M-C, Burke B, Haudenschild C: Preservation of thrombomodulin antigen on vascular and extravascular surfaces. J Histochem Cytochem 35:1267, 1987
2. Imada M, Imada S, Iwasaki H, Kume A, Yamaguchi H, Moore E: Fetomodulin: Marker surface protein of fetal development which is modulatable by cyclic AMP. Dev Biol 122:483, 1987
3. Imada S, Yamaguchi H, Nagumo M, Katayanagi S, Iwasaki H, Imada M: Identification of fetomodulin, a surface marker protein of fetal development, as thrombomodulin by gene cloning and functional assays. Dev Biol 140:113, 1990
4. Esmon C: The roles of protein C and thrombomodulin in the regulation of blood coagulation. J Biol Chem 264:4743, 1989
5. Esmon C: Thrombomodulin as a model of molecular mechanisms that modulate protease specificity and function at the vessel surface. FASEB J 9:946, 1995
6. Bovill EG, Bauer KA, Dickerman JD, Callas P, West B: The clinical spectrum of heterozygous protein C deficiency in a large New England kindred. Blood 73:712, 1989
7. Svensson P, Dahlback B: Resistance to activated protein C as a basis for venous thrombosis. N Engl J Med 330:517, 1994
8. Ohlin A-K, Norlund L, Marlar R: Thrombomodulin gene variations and thromboemboic disease. Thromb Haemost 78:396, 1997
9. Bajzar L, Manuel R, Nesheim M: Purification and characterization of TAFI, a thrombin-activatable fibrinolysis inhibitor. J Biol Chem 270:14477, 1995
10. Healy A. Rayburn H, Rosenberg R, Weiler H: Absence of the blood-clotting regulator thrombomodulin causes embryonic lethality in mice before development of a functional cardiovascular system. Proc Natl Acad Sci USA 92:850, 1995
11. Weiler-Guettler H, Christie P, Beeler D, Healy A, Hancock W, Rayburn H, Edelberg J, Rosenberg R: A targeted point mutation in thrombomodulin generates viable mice with a prethrombotic state. J Clin Invest 101:1, 1998
12. Rosenberg R: Thrombomodulin gene disruption and mutation in mice. Thromb Haemost 78:705, 1997
13. Jackman RW, Beeler DL, Fritze L, Soff G, Rosenberg RD: Human thrombomodulin gene is intron depleted: Nucleic acid sequences of the cDNA and gene predict protein structure and suggest sites of regulatory control. Proc Natl Acad Sci USA 84:6425, 1987
14. Kurosawa S, Galvin J, Esmon N, Esmon C: Proteolytic formation and properties of functional domains of thrombomodulin. J Biol Chem 262:2206, 1987
15. Wen D, Dittman WA, Ye RD, Deaven LL, Majerus PW, Sadler JE: Human thrombomodulin: Complete cDNA sequence and chromosome localization of the gene. Biochemistry 26:4350, 1987
16. Petersen T: The amino-terminal domain of thrombomodulin and pancreatic stone protein are homologous with lectins. FEBS Lett 231:51, 1988
17. Patthy L: Detecting distant homologies of mosaic proteins. Analysis of the sequences of thrombomodulin, thrombospondin, complement components C9, C8 alpha and C8 beta, vitronectin and plasma cell membrane glycoprotein PC-1. J Mol Biol 202:689, 1988
18. McEver R: Leukocyte interactions mediated by selectins. Thromb Haemost 66:80, 1991
19. Conway E, Pollefeyt S, Collen D, Steiner-Mosonyi M: The amino terminal lectin-like domain of thrombomodulin is required for constitutive endocytosis. Blood 89:652, 1997
20. Conway E, Nowakowski B, Steiner-Mosonyi M: Thrombomodulin lacking the cytoplasmic domain efficiently internalizes thrombin via nonclathrin-coated, pit-mediated endocytosis. J Cell Physiol 158:285, 1994
21. Teasdale M, Bird C, Bird P: Internalization of the anticoagulant thrombomodulin is constitutive and does not require a signal in the cytoplasmic domain. Immunol Cell Biol 72:480, 1994
22. Zhang Y, Weiler-Guettler H, Chen J, Wilhelm O, Deng Y, Qiu F, Nakagawa K, Klevesath M, Wilhelm S, Bohrer H, Nakagawa M, Graeff H. Martin E, Stern D, Rosenberg R, Ziegler R, Nawroth P: Thrombomodulin modulates growth of tumor cells independent of its anticoagulant activity. J Clin Invest 101:1301, 1998
23. Dittman W, Majerus P: Sequence of a cDNA for mouse thrombomodulin and comparison of the predicted mouse and human amino acid sequences. Nucleic Acids Res 17:802, 1989
24. Ford V, Kennel S: An intracisternal A-particle DNA sequence is closely linked to the thrombomodulin gene in some strains of laboratory mice. DNA Cell Biol 12:311, 1993
25. Fukushige S, Sauer B: Genomic targeting with a positive-selection lox integration vector allows highly reproducible gene expression in mammalian cells. Proc Natl Acad Sci USA 89:7905, 1992
26. Wood S, Allen N, Rossant J, Auerbach A, Nagy A: Non-injection methods for the production of embryonic stem cell-embryo chimaeras. Nature 365:87, 1993
27. Conway E, Boffa M, Nowakowski B, Steiner-Mosonyi M: An ultrastructural study of thrombomodulin endocytosis: Internalization occurs via clathrin-coated and non-coated pits. J Cell Physiol 151:604, 1992
28. Conway EM, Rosenberg RD: Tumor necrosis factor suppresses transcription of the thrombomodulin gene in endothelial cells. Mol Cell Biol 8:5588, 1988
29. Chomczynski P, Sacchi N: Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156, 1987
30. Kennel S, Lankford T, Hughes B, Hotchkiss J: Quantitation of a murine lung endothelial cell protein, P112, with a double monoclonal antibody assay. Lab Invest 59:692, 1988
31. Declerck P, Verstreken M, Collen D: Immunoassay of murine t-PA, u-PA and PAI-1 using monoclonal antibodies raised in geneinactivated mice. Thromb Haemost 74:1305, 1995
32. Lijnen H, Van Hoef B, Collen D: Characterization of the murine plasminogen/urokinase-type plasminogen-activator system. Eur J Biochem 241:840, 1996
33. Marglin A, Merrifield R: Chemical synthesis of peptides and proteins. Annu Rev Biochem 39:841, 1970
34. Laemmli V: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680, 1970
35. Conway E, Nowakowski B: Biologically active thrombomodulin is synthesized by adherent synovial fluid cells and is elevated in synovial fluid of patients with rheumatoid arthritis. Blood 81:726, 1993
36. Lawson C, Yan S, Yan S, Liao H, Zhou Y, Sobel J, Kisiel W, Stern D, Pinsky D: Monocytes and tissue factor promote thrombosis in a murine model of oxygen deprivation. J Clin Invest 99:1729, 1997
37. Esmon C, Taylor F, Snow T: Inflammation and coagulation: Linked processes potentially mediated by protein C. Thromb Haemost 66:160, 1991
38. Conway E, Liu L, Nowakowski B, Steiner-Mosonyi M, Jackman R: Heat shock of vascular endothelial cells induces an upregulatory transcriptional response of the thrombomodulin gene that is delayed in onset and does not attenuate. J Biol Chem 269:22804, 1994
39. Raife TJ, Lager DJ, Madison KC, Piette WW, Howard EJ, Sturm MT, Chen Y, Lentz SR: Thrombomodulin expression by human keratinocytes. Induction of cofactor activity during epidermal differentiation. J Clin Invest 93:1846, 1994
40. Nesheim M, Wang W, Boffa M, Nagashima M, Morser J, Bajzar L: Thrombin, thrombomodulin and TAFI in the molecular link between coagulation and fibrinolysis. Thromb Haemost 78:386, 1997
41. Kokame K, Zheng X, Sadler J: Activation of thrombinactivatable fibrinolysis inhibitor requires epidermal growth factor-like domain 3 of thrombomodulin and is inhibited competitively by protein C. J Biol Chem 273:12135, 1998
42. Nawa K, Itani T, Ono M, Sakano K, Marumoto Y, Iwamoto M: The glycosaminoglycan of recombinant human soluble thrombomodulin affects antithrombotic activity in a rat model of tissue factor-induced disseminated intravascular coagulation. Thromb Haemost 67:366, 1992
43. Bajzar L, Morser J, Nesheim M: TAFI, or plasma procarboxypeptidase B, couples the coagulation and fibrinolytic cascades through the thrombin-thrombomodulin complex. J Biol Chem 271:16603, 1996
44. Kramer M, Schaefer B, Reinartz J: Plasminogen activation of human keratinocytes: molecular pathways and cell-biological consequences. Biol Chem Hoppe Seyler 376:131, 1995
45. Romer J, Bugge T, Pyke C, Lund L, Flick M, Degen J, Dano K: Impaired wound healing in mice with a disrupted plasminogen gene. Nat Med 2:287, 1996
46. Bugge T, Kombrinck K, Flick M, Daugherty C, Danton M, Degen J: Loss of fibrinogen rescues mice from the pleiotropic effects of plasminogen deficiency. Cell 15:709, 1996
47. Raife T, Lager D, Peterson J, Erger R, Lentz S: Keratinocytespecific expression of human thrombomodulin in transgenic mice: Effects on epidermal differentiation and cutaneous wound healing. J Invest Med 46:127, 1998
48. Carmeliet P, Bouche A, De Clercq C, Janssen S, Pollefeyt S, Wyns S, Mulligan R, Collen D: Biological effects of disruption of tissue-type plasminogen activator, urokinase-type plasminogen activator, and plasminogen activator inhibitor-1 genes in mice. Ann NY Acad Sci 748:367, 1995
49. Grulich-Henn J, Müller-Berghaus G: Regulation of endothelial tissue plasminogen activator and plasminogen activator inhibitor type 1 synthesis by diacylglycerol, phorbol ester, and thrombin. Blut 61:38, 1990