Thrombomodulin in the treatment of atherothrombotic diseases

Frontiers in Bioscience - Scholar

Volumn 1 S, Issue 1, 2009, Pages 33-38

  Li, Yi Heng ^a   Shi, Guey Yueh ^a   Wu, Hua Lin ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

Atherosclerosis; Inflammation; Review; Thrombomodulin; Thrombosis

Indexed keywords

RECOMBINANT PROTEIN; THROMBOMODULIN;

ATHEROSCLEROSIS; HUMAN; REVIEW; THROMBOSIS;

ATHEROSCLEROSIS; HUMANS; RECOMBINANT PROTEINS; THROMBOMODULIN; THROMBOSIS;

EID: 77954515737     PISSN: 19450516     EISSN: 19450524     Source Type: Journal    
DOI: 10.2741/e4     Document Type: Review

References (53)

1. Esmon, C. T. The regulation of natural anticoagulant pathways. Science 235, 1348-52 (1987) (Pubitemid 17041653)
2. Esmon, C. T. The roles of protein C and thrombomodulin in the regulation of blood coagulation. J Biol Chem 264, 4743-6 (1989) (Pubitemid 19092874)
3. Dittman, W. A., Majerus, P. W. Structure and function of thrombomodulin. Blood 75, 329-33 (1990)
4. Stearns, D. J., Kurosawa, S., Esmon, C. T. Microthrombomodulin. Residues 310-486 from the epidermal growth factor precursor homology domain of thrombomodulin will accelerate protein C activation. J Biol Chem 264, 3352-6 (1989) (Pubitemid 19063390)
5. Zushi, M., Gomi, K., Yamamoto, S., Maruyama, I., Hayashi, T., Suzuki, K. The last three consecutive epidermal growth factor-like structures of human thrombomodulin comprise the minimum functional domain for protein C-activating cofactor activity and anticoagulant activity. J Biol Chem 264, 10351-3 (1989) (Pubitemid 19161593)
6. Soff, G. A., Jackman, R. W., Rosenberg, R. D. Expression of thrombomodulin by smooth muscle cells in culture: different effects of tumor necrosis factor and cyclic adenosine monophosphate on thrombomodulin expression by endothelial cells and smooth muscle cells in culture. Blood 77, 515-8 (1991)
7. Tohda. G., Oida. K., Okada. Y., Kosaka. S., Okada. E., Takahashi. S., Ishii. H., Miyamori. I. Expression of thrombomodulin in atherosclerotic lesions and mitogenic activity of recombinant thrombomodulin in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 18, 1861-9 (1998) (Pubitemid 28565747)
8. Li. Y. H., Hsieh. C. Y., Wang. D. L., Chung. H. C., Liu. S. L., Chao. T. H., Shi. G. Y., Wu. H. L. Remodeling of carotid arteries is associated with increased expression of thrombomodulin in a mouse transverse aortic constriction model. Thromb Haemost 97, 658-64 (2007) (Pubitemid 46592944)
9. Suzuki, K., Nishioka, J., Hayashi, T., Kosaka, Y. Functionally active thrombomodulin is present in human platelets. J Biochem (Tokyo) 104, 628-32 (1988)
10. McCachren. S. S., Diggs. J., Weinberg. J. B., Dittman. W. A. Thrombomodulin expression by human blood monocytes and by human synovial tissue lining macrophages. Blood 78, 3128-32 (1991)
11. Raife. T. J., Lager. D. J., Madison. K. C., Piette. W. W., Howard. E. J., Sturm. M. T., Chen. Y., Lentz. S. R. Thrombomodulin expression by human keratinocytes. Induction of cofactor activity during epidermal differentiation. J Clin Invest 93, 1846-51 (1994)
12. Suehiro. T., Shimada. M., Matsumata. T., Taketomi. A., Yamamoto. K., Sugimachi. K. Thrombomodulin inhibits intrahepatic spread in human hepatocellular carcinoma. Hepatology 21, 1285-90 (1995)
13. Ogawa. H., Yonezawa. S., Maruyama. I., Matsushita. Y., Tezuka. Y., Toyoyama. H., Yanagi. M., Matsumoto. H., Nishijima. H., Shimotakahara. T., Aikou. T., Sato. E. Expression of thrombomodulin in squamous cell carcinoma of the lung: its relationship to lymph node metastasis and prognosis of the patients. Cancer Lett 149, 95-103 (2000). (Pubitemid 30100565)
14. Hanly. A. M., Redmond. M., Winter. D. C., Brophy. S., Deasy. J. M., Bouchier-Hayes. D. J., Kay. E. W. Thrombomodulin expression in colorectal carcinoma is protective and correlates with survival. Br J Cancer 94, 1320-5 (2006)
15. Liu. L. W., Vu. T. K., Esmon. C. T., Coughlin. S. R. The region of the thrombin receptor resembling hirudin binds to thrombin and alters enzyme specificity. J Biol Chem 266, 16977-80 (1991) (Pubitemid 21907892)
16. Ye. J., Liu. L. W., Esmon. C. T., Johnson. A. E. The fifth and sixth growth factor-like domains of thrombomodulin bind to the anion-binding exosite of thrombin and alter its specificity. J Biol Chem 267, 11023-8 (1992)
17. Ossovskaya. V. S., Bunnett. N. W. Protease-activated receptors: contribution to physiology and disease. Physiol Rev 84, 579-621 (2004) (Pubitemid 38365493)
18. Sturn. D. H., Kaneider. N. C., Feistritzer. C., Djanani. A., Fukudome. K., Wiedermann. C. J. Expression and function of the endothelial protein C receptor in human neutrophils. Blood 102, 1499-505 (2003) (Pubitemid 36988062)
19. Yuksel. M., Okajima. K., Uchiba. M., Horiuchi. S., Okabe. H. Activated protein C inhibits lipopolysaccharideinduced tumor necrosis factor-alpha production by inhibiting activation of both nuclear factor-kappa B and activator protein-1 in human monocytes. Thromb Haemost 88, 267-73 (2002) (Pubitemid 34873708)
20. Bernard. G. R., Vincent. J. L., Laterre. P. F., LaRosa. S. P., Dhainaut. J. F., Lopez-Rodriguez. A., Steingrub. J. S., Garber. G. E., Helterbr. J. D., Ely. E. W., Fisher. C. J. The Recombinant Human Activated Protein C Worldwide Evaluation in Severe Sepsis (PROWESS) Study Group. Efficacy and safety of recombinant human activated protein C for severe sepsis. N Engl J Med 344, 699-709 (2001)
21. Bajzar. L., Morser. J., Nesheim. M. TAFI, or plasma procarboxypeptidase B, couples the coagulation and fibrinolytic cascades through the thrombinthrombomodulin complex. J Biol Chem 271, 16603-8 (1996) (Pubitemid 26239017)
22. Myles. T., Nishimura. T., Yun. T. H., Nagashima. M., Morser. J., Patterson. A. J., Pearl. R. G., Leung. L. L. Thrombin activatable fibrinolysis inhibitor, a potential regulator of vascular inflammation. J Biol Chem 278, 51059-67 (2003) (Pubitemid 38020340)
23. Weiler. H., Lindner. V., Kerlin. B., Isermann. B. H., Hendrickson. S. B., Cooley. B. C., Meh. D. A., Mosesson. M. W., Shworak. N. W., Post. M. J., Conway. E. M., Ulfman. L. H., von Andrian. U. H., Weitz. J. I. Characterization of a mouse model for thrombomodulin deficiency. Arterioscler Thromb Vasc Biol 21, 1531-7 (2001) (Pubitemid 34219820)
24. Conway. E. M., Van de Wouwer. M., Pollefeyt. S., Jurk. K., Van Aken. H., De Vriese. A., Weitz. J. I., Weiler. H., Hellings. P. W., Schaeffer. P., Herbert. J. M., Collen. D., Theilmeier. G. The lectin-like domain of thrombomodulin confers protection from neutrophil-mediated tissue damage by suppressing adhesion molecule expression via nuclear factor kappa. B and mitogen-activated protein kinase pathways. J Exp Med 196, 565-77 (2002) (Pubitemid 35024436)
25. Abeyama. K., Stern. D. M., Ito. Y., Kawahara. K., Yoshimoto. Y., Tanaka. M., Uchimura. T., Ida. N., Yamazaki. Y., Yamada. S., Yamamoto. Y., Yamamoto. H., Iino. S., Taniguchi. N., Maruyama. I. The N-terminal domain of thrombomodulin sequesters high-mobolity-B1 protein, a novel antiinflammatory mechanism. J Clin Invest 115, 1267-74 (2005) (Pubitemid 40629045)
26. Hamada. H., Ishii. H., Sakyo. K., Horie. S., Nishiki. K., Kazama. M. The epidermal growth factor-like domain of recombinant human thrombomodulin exhibits mitogenic activity for Swiss 3T3 cells. Blood 86, 225-33 (1995)
27. Li. Y. H., Shi. G. Y., Wu. H. L. The role of thrombomodulin in atherosclerosis: from bench to bedside. Cardiovasc Hematol Agents Med Chem 4, 183-7 (2006)
28. Grinnell. B. W., Berg. D. T. Surface thrombomodulin modulates thrombin receptor responses on vascular smooth muscle cells. Am J Physiol 270, H-603-9 (1996)
29. 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. M., Rosenberg. R. D., Ziegler. R., Nawroth. P. P. Thrombomodulin modulates growth of tumor cells independent of its anticoagulant activity. J Clin Invest 101, 1301-9 (1998) (Pubitemid 28166827)
30. Li. J., Garnette. C. S., Cahn. M., Claytor. R. B., Rohrer. M. J., Dobson. J. G Jr., Gerlitz. B., Cutler. B. S. Recombinant thrombomodulin inhibits arterial smooth muscle cell proliferation induced by thrombin. J Vasc Surg 32, 804-13 (2000)
31. Huang. H. C., Shi. G. Y., Jiang. S. J., Shi. C. S., Wu. C. M., Yang. H. Y., Wu. H. L. Thrombomodulin-mediated cell adhesion: involvement of its lectin-like domain. J Biol Chem 278, 46750-9 (2003)
32. Iino. S., Abeyama. K., Kawahara. K., Yamakuchi. M., Hashiguchi. T., Matsukita. S., Yonezawa. S., Taniguchi. S., Nakata. M., Takao. S., Aikou. T., Maruyama. I. The antimetastatic role of thrombomodulin expression in islet cell-derived tumors and its diagnostic value. Clin Cancer Res 10, 6179-88 (2004) (Pubitemid 39287524)
33. Mohri. M., Suzuki. M., Sugimoto. E., Sata. M., Yamamoto. S., Maruyama. I. Effects of recombinant human soluble thrombomodulin (rhs-TM) on clotinduced coagulation in human plasma. Thromb Haemost 80, 925-9 (1998) (Pubitemid 28556694)
34. Gomi, K., Zushi, M., Honda, G., Kawahara, S., Matsuzaki, O., Kanabayashi, T., Yamamoto, S., Maruyama, I., Suzuki, K. Antithrombotic effect of recombinant human thrombomodulin on thrombininduced thromboembolism in mice. Blood 75, 1396-9 (1990) (Pubitemid 20114874)
35. Aoki. Y., Takei. R., Mohri. M., Gonda. Y., Gomi. K., Sugihara. T., Kiyota. T., Yamamoto. S., Ishida. T., Maruyama. I. Antithrombotic effects of recombinant human soluble thrombomodulin (rhs-TM) on arteriovenous shunt thrombosis in rats. Am J Hematol 47, 162-6 (1994) (Pubitemid 24333441)
36. Mohri. M., Gonda. Y., Oka. M., Aoki. Y., Gomi. K., Kiyota. T., Sugihara. T., Yamamoto. S., Ishida. T., Maruyama. I. The antithrombotic effects of recombinant human soluble thrombomodulin (rhsTM) on tissue factorinduced disseminated intravascular coagulation in crabeating monkeys (Macaca fascicularis). Blood Coagul Fibrinolysis 8, 274-83 (1997) (Pubitemid 27360009)
37. Tanaka. K. A., Fernandez. J. A., Marzec. U. M., Kelly. A. B., Mohri. M., Griffin. J. H., Hanson. S. R., Gruber. A. Soluble thrombomodulin is antithrombotic in the presence of neutralising antibodies to protein C and reduces circulating activated protein C levels in primates. Br J Haematol 132, 197-203 (2006) (Pubitemid 43381553)
38. Nakashima. M., Kanamaru. M., Umemura. K., Tsuruta. K. Pharmacokinetics and safety of a novel recombinant soluble human thrombomodulin, ART-123, in healthy male volunteers. J Clin Pharmacol 38, 40-4 (1998) (Pubitemid 28086722)
39. Moll. S., Lindley. C., Pescatore. S., Morrison. D., Tsuruta. K., Mohri. M., Serada. M., Sata. M., Shimizu. H., Yamada. K., White. G. C. 2nd. Phase I study of a novel recombinant human soluble thrombomodulin, ART-123. J Thromb Haemost 2, 1745-51 (2004) (Pubitemid 40192715)
40. Kearon. C., Comp. P., Douketis. J., Royds. R., Yamada. K., Gent. M. Dose-response study of recombinant human soluble thrombomodulin (ART-123) in the prevention of venous thromboembolism after total hip replacement. J Thromb Haemost 3, 962-8 (2005) (Pubitemid 41632827)
41. Saito. H., Maruyama. I., Shimazaki. S., Yamamoto. Y., Aikawa. N., Ohno. R., Hirayama. A., Matsuda. T., Asakura. H., Nakashima. M., Aoki. N. Efficacy and safety of recombinant human soluble thrombomodulin (ART-123) in disseminated intravascular coagulation: results of a phase III, randomized, double-blind clinical trial. J Thromb Haemost 5, 31-41 (2007) (Pubitemid 44921064)
42. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 352, 1685-95 (2005)
43. Laszik. Z. G., Zhou. X. J., Ferrell. G. L., Silva. F. G., Esmon. C. T. Down-regulation of endothelial expression of endothelial cell protein C receptor and thrombomodulin in coronary atherosclerosis. Am J Pathol 159, 797-802 (2001) (Pubitemid 32847169)
44. Li. Y. H., Chen. J. H., Wu. H. L., Shi. G. Y., Huang. H. C., Chao. T. H., Tsai. W. C., Tsai. L. M., Guo. H. R., Wu. W. S., Chen. Z. C. G-33A mutation in the promoter region of thrombomodulin gene and its association with coronary artery disease and plasma soluble thrombomodulin levels. Am J Cardiol 85, 8-12 (2000)
45. Li. Y. H., Chen. C. H., Yeh. P. S., Lin. H. J., Chang. B. I., Lin. J. C., Guo. H. R., Wu. H. L., Shi. G. Y., Lai. M. L., Chen. J. H. Functional mutation in the promoter region of thrombomodulin gene in relation to carotid atherosclerosis. Atherosclerosis 154, 713-9 (2001)
46. Waugh. J. M., Li-Hawkins. J., Yuksel. E., Kuo. M. D., Cifra. P. N., Hilfiker. P. R., Geske. R., Chawla. M., Thomas. J., Shenaq. S. M., Dake. M. D., Woo. S. L. Thrombomodulin overexpression to limit neointima formation. Circulation 102, 332-7 (2000) (Pubitemid 30457585)
47. Li. J. M., Singh. M. J., Itani. M., Vasiliu. C., Hendricks. G., Baker. S. P., Hale. J. E., Rohrer. M. J., Cutler. B. S., Nelson. P. R. Recombinant human thrombomodulin inhibits arterial neointimal hyperplasia after balloon injury. J Vasc Surg 39, 1074-83 (2004) (Pubitemid 38581640)
48. Li. Y. H., Liu. S. L., Shi. G. Y., Tseng. G. H., Liu. P. Y., Wu. H. L. Thrombomodulin plays an important role in arterial remodeling and neointima formation in mouse carotid ligation model. Thromb Haemost 95, 128-33 (2006)
49. Uchiba. M., Okajima. K., Murakami. K., Johno. M., Okabe. H., Takatsuki. K. Effect of human urinary thrombomodulin on endotoxin-induced intravascular coagulation and pulmonary vascular injury in rats. Am J Hematol 54, 118-23 (1997) (Pubitemid 27079417)
50. Ikeguchi. H., Maruyama. S., Morita. Y., Fujita. Y., Kato. T., Natori. Y., Akatsu. H., Campbell. W., Okada. N., Okada. H., Yuzawa. Y., Matsuo. S. Effects of human soluble thrombomodulin on experimental glomerulonephritis. Kidney Int 61, 490-501 (2002) (Pubitemid 34102589)
51. Mohri. T., Tanaka. H., Tajima. G., Kajino. K., Sonoi. H., Hosotsubo. H., Ogura. H., Kuwagata. Y., Shimazu. T., Sugimoto. H. Synergistic effects of recombinant human soluble thrombomodulin and fluid-volume resuscitation in a rat lethal crush injury model. Shock 26, 581-6 (2006) (Pubitemid 44789632)
52. Taoka. Y., Okajima. K., Uchiba. M., Johno. M. Neuroprotection by recombinant thrombomodulin. Thromb Haemost 83, 462-8 (2000) (Pubitemid 30148362)
53. van de Wouwer M., Plaisance. S., De Vriese. A., Waelkens. E., Collen. D., Persson. J., Daha. M. R., Conway. E. M. The lectin-like domain of thrombomodulin interferes with complement activation and protects against arthritis. J Thromb Haemost 4, 1813-24 (2006) (Pubitemid 44144810)