Coagulation factor Xa signaling: the link between coagulation and inflammatory bowel disease?

Trends in Pharmacological Sciences

Volumn 30, Issue 1, 2009, Pages 8-16

  Borensztajn, Keren ^a,b   Peppelenbosch, Maikel P ^a   Spek, C Arnold ^b  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CLOTTING FACTOR 10A; PROTEINASE ACTIVATED RECEPTOR; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; PROTEINASE ACTIVATED RECEPTOR 3; PROTEINASE ACTIVATED RECEPTOR 4;

ARTICLE; BLOOD CLOTTING; CELL PROLIFERATION; DISEASE COURSE; ENTERITIS; FIBROBLAST; HUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION;

ANIMALS; BLOOD COAGULATION; FACTOR XA; HUMANS; INFLAMMATORY BOWEL DISEASES; MODELS, BIOLOGICAL; RECEPTORS, PROTEINASE-ACTIVATED; SIGNAL TRANSDUCTION;

EID: 58149120812     PISSN: 01656147     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tips.2008.10.007     Document Type: Article

References (81)

1. Baumgart D.C., and Carding S.R. Inflammatory bowel disease: cause and immunobiology. Lancet 369 (2007) 1627-1640
2. Strober W., et al. The fundamental basis of inflammatory bowel disease. J. Clin. Invest. 117 (2007) 514-521
3. Rieder F., et al. Wound healing and fibrosis in intestinal disease. Gut 56 (2007) 130-139
4. Trousseau A. Phlegmasia alba dolens. Clinique medicale de l'Hotel-Dieu de Paris (1865) 654-712
5. Danese S., et al. Inflammation and coagulation in inflammatory bowel disease: the clot thickens. Am. J. Gastroenterol. 102 (2007) 174-186
6. Hollenberg M.D., and Compton S.J. International Union of Pharmacology. XXVIII. Proteinase-activated receptors. Pharmacol. Rev. 54 (2002) 203-217
7. Vergnolle N. Modulation of visceral pain and inflammation by protease-activated receptors. Br. J. Pharmacol. 141 (2004) 1264-1274
8. Steinhoff M., et al. Proteinase-activated receptors: transducers of proteinase-mediated signaling in inflammation and immune response. Endocr. Rev. 26 (2005) 1-43
9. Ramachandran R., and Hollenberg M.D. Proteinases and signalling: pathophysiological and therapeutic implications via PARs and more. Br. J. Pharmacol. 153 Suppl. 1 (2008) S263-S282
10. Ruf W., et al. Specificity of coagulation factor signaling. J. Thromb. Haemost. 1 (2003) 1495-1503
11. Chambers R.C. Role of coagulation cascade proteases in lung repair and fibrosis. Eur. Respir. J. Suppl. 44 (2003) 33s-35s
12. Napoli C., et al. Evidence that protease activated receptor 2 expression is enhanced in human coronary atherosclerotic lesions. J. Clin. Pathol. 57 (2004) 513-516
13. Tennant G.M., et al. PAR-2 mediates increased inflammatory cell adhesion and neointima formation following vascular injury in the mouse. Atherosclerosis 198 (2008) 57-64
14. Chambers R.C., and Laurent G.J. Coagulation cascade proteases and tissue fibrosis. Biochem. Soc. Trans. 30 (2002) 194-200
15. Levi-Schaffer F., and Piliponsky A.M. Tryptase, a novel link between allergic inflammation and fibrosis. Trends Immunol. 24 (2003) 158-161
16. Cederqvist K., et al. High expression of pulmonary proteinase-activated receptor 2 in acute and chronic lung injury in preterm infants. Pediatr. Res. 57 (2005) 831-836
17. Masamune A., et al. Protease-activated receptor-2-mediated proliferation and collagen production of rat pancreatic stellate cells. J. Pharmacol. Exp. Ther. 312 (2005) 651-658
18. Vesey D.A., et al. Potential physiological and pathophysiological roles for protease-activated receptor-2 in the kidney. Nephrology (Carlton) 12 (2007) 36-43
19. Nishibori M., et al. Physiology and pathophysiology of proteinase-activated receptors (PARs): PAR-2-mediated proliferation of colon cancer cell. J. Pharmacol. Sci. 97 (2005) 25-30
20. Antalis T.M., et al. Mechanisms of disease: protease functions in intestinal mucosal pathobiology. Nat. Clin. Pract. Gastroenterol. Hepatol. 4 (2007) 393-402
21. Kawabata A., et al. Gastrointestinal roles for proteinase-activated receptors in health and disease. Br. J. Pharmacol. 153 Suppl. 1 (2008) S230-S240
22. Kong W., et al. Luminal trypsin may regulate enterocytes through proteinase-activated receptor 2. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 8884-8889
23. Buresi M.C., et al. Protease-activated receptor-1 stimulates Ca(2+)-dependent Cl(-) secretion in human intestinal epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 281 (2001) G323-G332
24. Wang J., et al. Deficiency of microvascular thrombomodulin and up-regulation of protease-activated receptor-1 in irradiated rat intestine: possible link between endothelial dysfunction and chronic radiation fibrosis. Am. J. Pathol. 160 (2002) 2063-2072
25. Seymour M.L., et al. PAR1-dependent and independent increases in COX-2 and PGE2 in human colonic myofibroblasts stimulated by thrombin. Am. J. Physiol. Cell Physiol. 284 (2003) C1185-C1192
26. Buresi M.C., et al. Activation of proteinase-activated receptor-1 inhibits neurally evoked chloride secretion in the mouse colon in vitro. Am. J. Physiol. Gastrointest. Liver Physiol. 288 (2005) G337-G345
27. Jarry A., et al. PAR-2 activation increases human intestinal mucin secretion through EGFR transactivation. Biochem. Biophys. Res. Commun. 364 (2007) 689-694
28. Nystedt S., et al. The proteinase-activated receptor 2 is induced by inflammatory mediators in human endothelial cells. Comparison with the thrombin receptor. J. Biol. Chem. 271 (1996) 14910-14915
29. Corvera C.U., et al. Thrombin and mast cell tryptase regulate guinea-pig myenteric neurons through proteinase-activated receptors-1 and -2. J. Physiol. 517 (1999) 741-756
30. Cenac N., et al. Proteinase-activated receptor-1 is an anti-inflammatory signal for colitis mediated by a type 2 immune response. Inflamm. Bowel Dis. 11 (2005) 792-798
31. Kawabata A., et al. A protective role of protease-activated receptor 1 in rat gastric mucosa. Gastroenterology 126 (2004) 208-219
32. Kim J.A., et al. Expression of protease-activated receptor 2 in ulcerative colitis. Inflamm. Bowel Dis. 9 (2003) 224-229
33. Gecse K., et al. Increased faecal serine protease activity in diarrhoeic IBS patients: a colonic lumenal factor impairing colonic permeability and sensitivity. Gut 57 (2008) 591-599
34. Cenac N., et al. Induction of intestinal inflammation in mouse by activation of proteinase-activated receptor-2. Am. J. Pathol. 161 (2002) 1903-1915
35. Nguyen C., et al. Colitis induced by proteinase-activated receptor-2 agonists is mediated by a neurogenic mechanism. Can. J. Physiol. Pharmacol. 81 (2003) 920-927
36. Hansen K.K., et al. A major role for proteolytic activity and proteinase-activated receptor-2 in the pathogenesis of infectious colitis. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 8363-8368
37. Roka R., et al. Dexamethasone prevents visceral hyperalgesia but not colonic permeability increase induced by luminal protease-activated receptor-2 agonist in rats. Gut 56 (2007) 1072-1078
38. Cenac N., et al. Role for protease activity in visceral pain in irritable bowel syndrome. J. Clin. Invest. 117 (2007) 636-647
39. Hyun E., et al. Protease-activated receptor-2 activation: a major actor in intestinal inflammation. Gut 57 (2008) 1222-1229
40. Steinhoff M., et al. Agonists of proteinase-activated receptor 2 induce inflammation by a neurogenic mechanism. Nat. Med. 6 (2000) 151-158
41. Amadesi S., and Bunnett N. Protease-activated receptors: protease signaling in the gastrointestinal tract. Curr. Opin. Pharmacol. 4 (2004) 551-556
42. Vergnolle N., et al. Proteinase-activated receptor-2 and hyperalgesia: a novel pain pathway. Nat. Med. 7 (2001) 821-826
43. Shpacovitch V., et al. Role of protease-activated receptors in inflammatory responses, innate and adaptive immunity. J. Leukoc. Biol. 83 (2008) 1309-1322
44. Yamada T., and Nagai Y. Immunohistochemical studies of human tissues with antibody to factor Xa. Histochem. J. 28 (1996) 73-77
45. Wojtukiewicz M.Z., et al. Indirect activation of blood coagulation in colon cancer. Thromb. Haemost. 62 (1989) 1062-1066
46. Hamill C.E., et al. Exacerbation of dopaminergic terminal damage in a mouse model of Parkinson's disease by the G-protein-coupled receptor protease-activated receptor 1. Mol. Pharmacol. 72 (2007) 653-664
47. Nomura K., et al. Roles of coagulation pathway and factor Xa in rat mesangioproliferative glomerulonephritis. Lab. Invest. 87 (2007) 150-160
48. Shinagawa K., et al. Coagulation factor Xa modulates airway remodeling in a murine model of asthma. Am. J. Respir. Crit. Care Med. 175 (2007) 136-143
49. Fiocchi C., et al. Alterations of mesenchymal and endothelial cells in inflammatory bowel diseases. Adv. Exp. Med. Biol. 579 (2006) 168-176
50. Danese S. Nonimmune cells in inflammatory bowel disease: from victim to villain. Trends Immunol. 29 (2008) 555-564
51. Papa A., et al. Vascular involvement in inflammatory bowel disease: pathogenesis and clinical aspects. Dig. Dis. 26 (2008) 149-155
52. Hatoum O.A., and Binion D.G. The vasculature and inflammatory bowel disease: contribution to pathogenesis and clinical pathology. Inflamm. Bowel Dis. 11 (2005) 304-313
53. Koizumi M., et al. Expression of vascular adhesion molecules in inflammatory bowel disease. Gastroenterology 103 (1992) 840-847
54. Riewald M., and Ruf W. Mechanistic coupling of protease signaling and initiation of coagulation by tissue factor. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 7742-7747
55. Hezi-Yamit A., et al. Synergistic induction of tissue factor by coagulation factor Xa and TNF: evidence for involvement of negative regulatory signaling cascades. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 12077-12082
56. Daubie V., et al. Factor Xa and thrombin evoke additive calcium and proinflammatory responses in endothelial cells subjected to coagulation. Biochim. Biophys. Acta 1763 (2006) 860-869
57. Senden N.H., et al. Factor Xa induces cytokine production and expression of adhesion molecules by human umbilical vein endothelial cells. J. Immunol. 161 (1998) 4318-4324
58. McLean K., et al. FXa-induced responses in vascular wall cells are PAR-mediated and inhibited by ZK-807834. Thromb. Res. 103 (2001) 281-297
59. Feistritzer C., et al. Protease-activated receptors-1 and -2 can mediate endothelial barrier protection: role in factor Xa signaling. J. Thromb. Haemost. 3 (2005) 2798-2805
60. Olanders K., et al. Effects of anticoagulant treatment on intestinal ischaemia and reperfusion injury in rats. Acta Anaesthesiol. Scand. 49 (2005) 517-524
61. Riewald M., et al. Gene induction by coagulation factor Xa is mediated by activation of protease-activated receptor 1. Blood 97 (2001) 3109-3116
62. Borensztajn K.S., et al. Coagulation factor Xa drives tumor cells into apoptosis through BH3-only protein Bim up-regulation. Exp. Cell Res. 313 (2007) 2622-2633
63. Flynn A.N., and Buret A.G. Proteinase-activated receptor 1 (PAR-1) and cell apoptosis. Apoptosis 9 (2004) 729-737
64. Suzuki T., et al. Proteinase-activated receptor-1 mediates elastase-induced apoptosis of human lung epithelial cells. Am. J. Respir. Cell Mol. Biol. 33 (2005) 231-247
65. Edelblum K.L., et al. Regulation of apoptosis during homeostasis and disease in the intestinal epithelium. Inflamm. Bowel Dis. 12 (2006) 413-424
66. Begue B., et al. Implication of TNF-related apoptosis-inducing ligand in inflammatory intestinal epithelial lesions. Gastroenterology 130 (2006) 1962-1974
67. Milia A.F., et al. TNFalpha blockade prevents the development of inflammatory bowel disease in HLA-B27 transgenic rats. J. Cell. Mol. Med. (2008) 10.1111/j.1582-4934.2008.00310.x
68. Mizoguchi E., et al. TNF receptor type I-dependent activation of innate responses to reduce intestinal damage-associated mortality. Gastroenterology 134 (2008) 470-480
69. Vetrano S., et al. Unique role of junctional adhesion molecule-a in maintaining mucosal homeostasis in inflammatory bowel disease. Gastroenterology 135 (2008) 173-184
70. Blanc-Brude O.P., et al. Factor Xa stimulates fibroblast procollagen production, proliferation, and calcium signaling via PAR1 activation. Exp. Cell Res. 304 (2005) 16-27
71. Bachli E.B., et al. Factor Xa and thrombin, but not factor VIIa, elicit specific cellular responses in dermal fibroblasts. J. Thromb. Haemost. 1 (2003) 1935-1944
72. Borensztajn K., et al. Factor Xa stimulates proinflammatory and profibrotic responses in fibroblasts via protease-activated receptor-2 activation. Am. J. Pathol. 172 (2008) 309-320
73. Seymour M.L., et al. Expression of proteinase-activated receptor 2 on human primary gastrointestinal myofibroblasts and stimulation of prostaglandin synthesis. Can. J. Physiol. Pharmacol. 83 (2005) 605-616
74. Burke J.P., et al. Fibrogenesis in Crohn's disease. Am. J. Gastroenterol. 102 (2007) 439-448
75. Pucilowska J.B., et al. IGF-I and procollagen alpha1(I) are coexpressed in a subset of mesenchymal cells in active Crohn's disease. Am. J. Physiol. Gastrointest. Liver Physiol. 279 (2000) G1307-G1322
76. Ketabchi S., et al. Expression of protease-activated receptor-1 and -2 in orofacial granulomatosis. Oral Dis. 13 (2007) 419-425
77. Grandaliano G., et al. Protease-activated receptor-2 expression in IgA nephropathy: a potential role in the pathogenesis of interstitial fibrosis. J. Am. Soc. Nephrol. 14 (2003) 2072-2083
78. Damiano B.P., et al. Cardiovascular responses mediated by protease-activated receptor-2 (PAR-2) and thrombin receptor (PAR-1) are distinguished in mice deficient in PAR-2 or PAR-1. J. Pharmacol. Exp. Ther. 288 (1999) 671-678
79. Vallance B.A., et al. TGF-beta1 gene transfer to the mouse colon leads to intestinal fibrosis. Am. J. Physiol. Gastrointest. Liver Physiol. 289 (2005) G116-G128
80. Tomasek J.J., et al. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat. Rev. Mol. Cell Biol. 3 (2002) 349-363
81. Kubo H., et al. Anticoagulant therapy for idiopathic pulmonary fibrosis. Chest 128 (2005) 1475-1482