Eosinophil cationic granule proteins impair thrombomodulin function: A potential mechanism for thromboembolism in hypereosinophilic heart disease

Journal of Clinical Investigation

Volumn 91, Issue 4, 1993, Pages 1721-1730

  Slungaard, Arne ^a   Vercellotti, Gregory M ^a   Tran, Thinh ^a   Gleich, Gerald J ^b   Key, Nigel S ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b MAYO CLINIC   (United States)

Author keywords

Cationic protein; Eosinophil cationic protein; Eosinophil peroxidase; Eosinophils; Glycosaminoglycan; Major basic protein; Thrombomodulin

Indexed keywords

CELL PROTEIN; CHONDROITIN SULFATE; GLYCOSAMINOGLYCAN; HEPARIN; MAJOR BASIC PROTEIN; PROTEIN C; THROMBOMODULIN;

AGED; ANIMAL CELL; ARTICLE; CASE REPORT; CONTROLLED STUDY; ENDOCARDITIS; EOSINOPHIL; EOSINOPHILIA; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOKALEMIA; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SWINE; THROMBOEMBOLISM;

AGED; BLOOD PROTEINS; ENDOCARDITIS; ENDOTHELIUM; EOSINOPHILIA; HEART DISEASES; HUMAN; MALE; MEMBRANE GLYCOPROTEINS; POTASSIUM; PROTEIN C; RECEPTORS, CELL SURFACE; RECEPTORS, THROMBIN; SUPPORT, NON-U.S. GOV'T; SUPPORT, U.S. GOV'T, P.H.S.; THROMBIN; THROMBOEMBOLISM;

EID: 0027175429     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI116382     Document Type: Article

References (50)

1. Parrillo, J. E., J. S. Borer, W. L. Henry, S. M. Wolff, and A. S. Fauci. 1979. The cardiovascular manifestations of the hypereosinophilic syndrome: prospective study of 26 patients, with review of the literature. Am. J. Med. 67:572-582.
2. Fauci, A. S., J. B. Harley, W. C. Roberts, V. J. Ferrans, H. R. Gralnick, and B. H. Bjornson. 1982. The idiopathic hypereosinophilic syndrome: clinical, pathophysiologic, and therapeutic considerations. Ann. Intern. Med. 97:78-92.
3. Oakley, C. M., and E. G. J. Olsen. 1977. Eosinophilia and heart disease. Br. Heart J. 39:233-237.
4. Bertrand, E., G. Cherian, S. K., Das, C. Dubost, A. O. Falase, F. Chi, J. F. Goodwin, J. Gvozdjak, C. Kawai, I. E. Mukharliamov. and E. G. J. Olsen. 1984. Cardiomyopathies: report of a WHO Expert Committee, Geneva. W HO Tech. Rep. Ser. 697:57-68.
5. Gleich, G. J., and C. R. Adolphson. 1986. The eosonophilic leukocyte: structure and function. Adv. Immunol. 39:177-253.
6. Spry, C. J. F., and P. C. Tai. 1976. Studies on blood eosinophils. II. Patients with Löffler's cardiopathy. Clin. Exp. Immunol. 24:423-434.
7. Wassom, D. L., D. A. Loegering, G. O. Solley, S. B. Moore, R. T. Schooley. A. S. Fauci, and G. J. Gleich. 1981. Elevated serum levels of the eosinophil granule major basic protein in patients with eosinophilia. J. Clin. Invest. 67:651-661.
8. Tai, P.-C. C. J. F. Spry, E. G. J. Olsen, S. J. Ackerman, S. Dunnette, and G. J. Gleich. 1987. Deposits of eosinophil granule proteins in cardiac tissues of patients with eosinophilic endomyocardial disease. Lancet. 1:643-647.
9. Slungaard. A., and Mahoney, J. R. 1991. Bromide-dependent toxicity of eosinophil peroxidase for endothelium and isolated working rat hearts: a model for eosinophilic endocarditis. J. Exp. Med. 173:117-126.
10. Maruyama, I., C. E. Bell, and P. W. Majerus. 1985. Thrombomodulin is found on endothelium of arteries, veins, capillaries, and lymphatics, and on syncytiotrophoblast of human placenta. J. Cell Biol. 101:363-371.
11. Esmon, C. T. 1989. The roles of protein C and thrombomodulin in the regulation of blood coagulation. J. Biol. Chem. 264:4743-4746.
12. Dittman, W. A., and P. W. Majerus. 1990. Structure and function of thrombomodulin: a natural anticoagulant. Blood. 75:329-336.
13. Kurosawa, S., and N. Aoki. 1985. Preparation of thrombomodulin from human placentas. Thromb. Res. 37:353-364.
14. Bourin, M.-C, E. Lundgren-Akerlund, and U. Lindahl. 1990. Isolation and characterization of the glycosaminoglycan component of rabbit thrombomodulin proteoglycan. J. Biol. Chem. 265:15424-15431.
15. Nawa, K., K.-I. Sakano, H. Fujiwara, Y. Sato, N. Sugiyama, T. Teruuchi, M. Iwamoto, and Y. Marumoto. 1990. Presence and function of chondroitin-4-sulfate on recombinant human soluble thrombomodulin. Biochem. Biophys. Res. Commun. 171:729-737.
16. Bourin, M.-C., M.-C Boffa, I. Björk, and U. Lindahl. 1986. Functional domains of rabbit thrombomodulin. Proc. Natl. Acad. Sci. USA. 83:5924-5928.
17. Bourin, M.-C., A.-K. Öhlin, D. A. Lane, J. Stenflo, and U. Lindahl. 1988. Relationship between anticoagulant activities and polyanionic properties of rabbit thrombomodulin. J. Biol. Chem. 263:8044-8052.
18. Preissner, K. T., T. Koyama, D. Müller, J. Tschopp, and G. Müller-Berghaus. 1990. Domain structure of the endothelial cell receptor thrombomodulin as deduced from modulation of its anticoagulation functions: evidence for a glycosaminoglycan-dependent secondary binding site for thrombin. J. Biol. Chem. 265:4915-4922.
19. Koyama, T., J. F. Parkinson, N. Aoki, N. U. Bang, G. Müller-Berghaus, and K. T. Preissner. 1991. Relationship between post-translational glycosylation and anticoagulatn function of secretable recombinant mutants of human thrombomodulin. Br. J. Haematol. 78:515-522.
20. Parkinson, J. F., C. J. Vlahos, S. C. B. Yan, and N. U. Bang. 1992. Recombinant human thrombomodulin: regulation of cofactor activity and anticoagulant function by a glycosaminoglycan side chain. Biochem. J. 283:151-157.
21. Preissner, K. T., U. Delvos, and G. Müller-Berghaus. 1987. Binding of thrombin to thrombomodulin accelerates inhibition of the enzyme by antithrombin. III. Evidence for a heparin-independent mechanism. Biochemistry. 26:2521-2528.
22. Parkinson, J. F., B. W. Grinnell, R. E. Moore, J. Hoskins, C. J. Vlahos, and N. U. Bang. 1990. Stable expression of a secretable deletion mutant of recombinant human thrombomodulin in mammalian cells. J. Biol. Chem. 265:12602-12610.
23. Parkinson, J. F., J. G. N. Garcia, and N. U. Bang. 1990. Decreased thrombin affinity of cell-surface thrombomodulin following treatment of cultured endothelial cells with β-D-xyloside. Biochem. Biophys. Res. Commun. 169:177-183.
24. Gleich, G. J., D. A. Loegering, K. G. Mann, and J. E. Maldonado. 1976. Comparative properties of the Charcot-Leyden crystal protein and the major basic protein from human eosinophils. J. Clin. Invest. 57:633-640.
25. Slifman, N. R., D. A. Loegering, D. J. McKean, and G. J. Gleich. 1986. Ribonuclease activity associated with human eosinophil-derived neurotoxin and eosinophil cationic protein. J. Immunol. 137:2913-2917.
26. Ten, R. M., L. R. Pease, D. J. McKean, M. P. Bell, and G. J. Gleich. 1989. Molecular cloning of human eosinophil peroxidase. Evidence for the existence of a peroxidase multigene family. J. Exp. Med. 169:1757-1769.
27. Gimbrone, M. A., Jr., E. J. Sheflon, and S. A. Cruise. 1978. Isolation and primary culture of endothelial cells from human umbilical vessels. Journal of the Tissue Culture Association Manual. 4:813-847.
28. Slungaard, A., J. Ascensao, E. Zanjani, and H. S. Jacob. 1983. Pulmonary carcinoma with eosinophilia: demonstration of a tumor-derived eosinophilopoietic factor. N. Engl. J. Med. 309:778-781.
29. Peters, M. S., A. L. Schroeter, G. M. Kephart, and G. J. Gleich. 1983. Localization of eosinophil granule major basic protein in chronic urticaria. J. Invest. Dermatol. 81:39-43.
30. Esmon, C. T., and W. G. Owen. 1981. Identification of an endothelial cell cofactor for thrombin-calalyzed activation of protein C. Proc. Natl. Acad. Sci. USA. 78:2249-2252.
31. Conway, E. M., and R. D. Rosenberg. 1988. Tumor necrosis factor suppresses transcription of the thrombomodulin gene in endothelial cells. Mol. Cell. Biol. 8:5588-5592.
32. Larkin, J. M., W. C. Donzell, and R. G. W. Andersen. 1985. Modulation of intracellular potassium and ATP: effects on coated pit function in fibroblasts and hepatocytes. J. Cell. Physiol. 124:372-378.
33. Leatherbarrow, R. J. 1990. Using linear and non-linear regression to fit biochemical data. Trends Biochem. Sci. 15:455-458.
34. Gleich, G. J., D. A. Loegering, F. Kueppers, S. P. Bajaj. and K. G. Mann. 1974. Physiochemical and biological properties of the major basic protein from guinea pig eosinophil granules. J Exp. Med. 140:313-332.
35. Wassom, D. L., D. A. Loegering, G. O. Solley, S. B. Moore, R. T. Schooley, A. S. Fauci, and G. J. Gleich. 1981. Elevated serum levels of the eosinophil granule major basic protein in patients with eosinophilia. J. Clin. Invest. 67:651-661.
36. Dittman, W. A., T. Kumada, J. E. Sadler, and P. W. Majerus. 1988. The structure and function of mouse thrombomodulin: phorbol myristate acetate stimulates degradation and synthesis of thrombomodulin without affecting mRNA levels in hemangioma cells. J. Biol. Chem. 263:15815-15822.
37. Nawroth, P. P., and D. M. Stern. 1986. Modulation of endothelial cell hemostatic properties by tumor necrosis factor. J. Exp. Med. 163:740-745.
38. Moore, K. L., C. T. Esmon, and N. L. Esmon. 1989. Tumor necrosis factor leads to the internalization and degradation of thrombomodulin from the surface of bovine aortic endothelial cells in culture. Blood. 73:159-165.
39. Wasmoen, T. L., M. P. Bell, D. A. Loegering, G. J. Gleich, F. G. Prendergast, and D. J. McKean. 1988. Biochemical and amino acid sequence analysis of human eosinophil granule major basic protein. J. Biol. Chem. 263:12559-12563.
40. Habermann, E. 1972. Bee and wasp venoms. Science (Wash. DC). 177:314-322.
41. Suzuki, K., T. Hayashi, J. Nishioka, Y. Kosaka, M. Zushi, G. Honda, and S. Yamamoto. 1989. A domain composed of epidermal growth factor-like structures of human thrombomodulin is essential for thrombin binding and for protein C activation. J. Biol. Chem. 264:4872-4876.
42. Hayashi, T., M. Zushi, S. Yamamoto, and K. Suzuki. 1990. Further localization of binding sites for thrombin and protein C in human thrombomodulin. J. Biol. Chem. 265:20156-20159.
43. Ye, J.,N. L. Esmon, C. T. Esmon, and A. E. Johnson. 1991. The active site of thrombin is altered upon binding to thrombomodulin: two distinct structural changes are detected by fluorescence, but only one correlates with protein C activation. J. Biol. Chem. 266:23016-23021.
44. Scuderi, P., K. S. Lam, K. J. Ryan, E. Petersen, K. E. Sterling, P. R. Finley, C. G. Ray, D. J. Slymen, and S. E. Salmon. 1986. Raised serum levels of tumour necrosis factor in parasitic infections. Lancet. 2:1364-1365.
45. Slungaard, A., G. M. Vercellolti, G. Walker, R. D. Nelson, and H. S. Jacob. 1990. Tumor necrosis factor/α-cachectin stimulates eosinophil oxidant production and toxicity towards human endothelium. J. Exp. Med. 171:2025-2041.
46. Venge, P., R. Dahl, and R. Hällgren. 1979. Enhancement of F XII-dependent reactions by eosinophil cationic protein. Thromb. Res. 14:641-649.
47. Rohrbach, M. S., C. L. Wheatley, N. R. Slifman, and G. J. Gleich. 1990. Activation of platelets by eosinophil granule proteins. J. Exp. Med. 172:1271-1274.
48. Kurosawa, S., J. B. Glavin, N. L. Esmon, and C. T. Esmon. 1987. Proteolytic formation and properties of functional domains of thrombomodulin. J. Biol. Chem. 262:2206-2212.
49. Taylor, S., and J. Folkman. 1982. Protamine is an inhibitor of angiogenesis. Nature (Lond.). 297:307-312.
50. Maione, T. E., G. S. Gray, J. Petro, A. J. Hunt, A. L. Donner, S. I. Bauer, H. F. Carson, and R. J. Sharpe. 1990. Inhibition of angiogenesis by recombinant human platelet factor 4 and related peptides. Science (Wash. DC). 247:77-79.