Antithrombin controls tumor migration, invasion and angiogenesis by inhibition of enteropeptidase

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Luengo Gil, Ginés ^a   Calvo, María Inmaculada ^b   Martín Villar, Ester ^b   Águila, Sonia ^a   Bohdan, Nataliya ^a   Antón, Ana I ^a   Espín, Salvador ^a   Ayala De La Peña, Francisco ^a   Vicente, Vicente ^a   Corral, Javier ^a   Quintanilla, Miguel ^b   Martínez Martínez, Irene ^a  

^a HOSPITAL UNIVERSITARIO MORALES MESEGUER   (Spain)

^b INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; ANTITHROMBIN; ENTEROPEPTIDASE; PROTEIN BINDING;

A-549 CELL LINE; ANIMAL; CELL MOTION; DRUG EFFECTS; ENDOTHELIUM CELL; GENETICS; HT-29 CELL LINE; HUMAN; MOUSE; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PROTEIN CONFORMATION; TUMOR INVASION;

A549 CELLS; ANGIOGENESIS INHIBITORS; ANIMALS; ANTITHROMBINS; CELL MOVEMENT; ENDOTHELIAL CELLS; ENTEROPEPTIDASE; HT29 CELLS; HUMANS; MICE; NEOPLASM INVASIVENESS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 84976351917     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep27544     Document Type: Article

References (45)

1. Hoffmann, J. N. et al. Benefit/risk profile of high-dose antithrombin in patients with severe sepsis treated with and without concomitant heparin. Thromb. Haemost. 95, 850-856 (2006).
2. Oelschlager, C. et al. Antithrombin III inhibits nuclear factor kappaB activation in human monocytes and vascular endothelial cells. Blood 99, 4015-4020 (2002).
3. Kienast, J. et al. Treatment effects of high-dose antithrombin without concomitant heparin in patients with severe sepsis with or without disseminated intravascular coagulation. J. Thromb. Haemost. 4, 90-97 (2006).
4. Warren, B. L. et al. Caring for the critically ill patient. High-dose antithrombin III in severe sepsis: a randomized controlled trial. JAMA. 286, 1869-1878 (2001).
5. O'Reilly, M. S., Pirie-Shepherd, S., Lane, W. S. & Folkman, J. Antiangiogenic activity of the cleaved conformation of the serpin antithrombin. Science 285, 1926-1928 (1999).
6. Larsson, H. et al. Antiangiogenic effects of latent antithrombin through perturbed cell-matrix interactions and apoptosis of endothelial cells. Cancer Res. 60, 6723-6729 (2000).
7. Prox, D. et al. Treatment of human pancreatic cancer in mice with angiogenic inhibitors. World J. Sug. 27, 405-411 (2003).
8. Asmal, M. et al. Inhibition of HCV by the serpin antithrombin III. Virol J. 9, 226 (2012).
9. Huang, C. Y., Sheen-Chen, S. M., Ho, H. T., Tang, R. P. & Eng, H. L. Antithrombin-III attenuates hepatocyte apoptosis in bile duct ligated rat: a striking cellular change. Surg. Innov. 17, 132-135 (2010).
10. Guerrero, J. A. et al. Protective role of antithrombin in mouse models of liver injury. J. Hepatol. 57, 980-986 (2012).
11. Choi, S. Y., Bertram, S., Glowacka, I., Park, Y. W. & Pöhlmann, S. Type II transmembrane serine proteases in cancer and viral infections. Trends Mol. Med. 15, 303-312 (2009).
12. Prohaska, T. A., Wahlmuller, F. C., Furtmuller, M. & Geiger, M. Interaction of protein C inhibitor with the type II transmembrane serine protease enteropeptidase. PLoS One 7, e39262 (2012).
13. Martinez-Martinez, I. et al. The infective polymerization of conformationally unstable antithrombin mutants may play a role in the clinical severity of antithrombin deficiency. Mol. Med. 18, 762-770 (2012).
14. Raja, S. M. et al. Deletion of P1 arginine in a novel antithrombin variant (antithrombin London) abolishes inhibitory activity but enhances heparin affinity and is associated with early onset thrombosis. J. Biol. Chem. 278, 13688-13695 (2003).
15. Martinez-Martinez, I. et al. Amelioration of the severity of heparin-binding antithrombin mutations by posttranslational mosaicism. Blood 120, 900-904 (2012).
16. Olson, S. T., Bjork, I. & Bock, S. C. Identification of critical molecular interactions mediating heparin activation of antithrombin: implications for the design of improved heparin anticoagulants. Trends Cardiovas. Med. 12, 198-205 (2002).
17. Martínez-Martínez, I. et al. Type II antithrombin deficiency caused by a large in-frame insertion: structural, functional, and pathlogical relevance. J. Thromb. Haemost. 10, 1859-1866 (2012).
18. Mushunje, A., Zhou, A., Carrel, R. W. & Huntington, J. A. Heparin-induced substrate behavior of antithrombin Cambridge II. Blood 102, 4028-4034 (2003).
19. Martin-Villar, E. et al. Podoplanin associates with CD44 to promote directional cell migration. Mol. Biol. Cell 21, 4387-4399 (2010).
20. Paz, H., Pathak, N. & Yang, J. Invading one step at a time: the role of invadopodia in tumor metastasis. Oncogene 33, 4193-4202 (2014).
21. Imamura, T. & Kitamoto, Y. Expression of enteropeptidase in differentiated enterocytes, goblet cells, and the tumor cells in human duodenum. Am. J. Physiol. Gastrointest. Liver Physiol. 285, G1235-1241 (2003).
22. Koivunen, E. et al. Tumor-Associated trypsin participates in cancer cell-mediated degradation of extracellular matrix. Cancer Res. 51, 2107-2112 (1991).
23. Vilen, S. T. et al. Intracellular co-localization of trypsin-2 and matrix metalloprotease-9: possible proteolytic cascade of trypsin-2, MMP-9 and enterokinase in carcinoma. Exp. Cell Res. 314, 914-926 (2008).
24. Zheng, X. L., Kitamoto, Y. & Sadler, J. E. Enteropeptidase, a type II transmembrane serine protease. Front Biosci. (Elite edition) 1, 242-249 (2009).
25. Franchini, M. & Mannucci, P. M. Low-molecular-weight heparins and cancer: focus on antitumoral effect. Ann. Med. 47, 116-121 (2015).
26. Lee, A. Y. et al. Randomized comparison of low molecular weight heparin and coumarin derivatives on the survival of patients with cancer and venous thromboembolism. J. Clin. Oncol. 23, 2123-2129 (2005).
27. Mousa, S. A. & Petersen, L. J. Anti-cancer properties of low-molecular-weight heparin: preclinical evidence. Thromb. Haemost. 102, 258-267 (2009).
28. von Tempelhoff, G. F. & Heilmann, L. Antithrombotic therapy in gynecologic surgery and gynecologic oncology. Hematol. Oncol. Clin. North Am. 14, 1151-1169 (2000).
29. Lazo-Langner, A., Goss, G. D., Spaans, J. N. & Rodger, M. A. The effect of low-molecular-weight heparin on cancer survival. A systematic review and meta-Analysis of randomized trials. J. Thromb. Haemost. 5, 729-737 (2007).
30. Nelson, R. M. et al. Heparin oligosaccharides bind L-And P-selectin and inhibit acute inflammation. Blood 82, 3253-3258 (1993).
31. Varki, N. M. & Varki A. Heparin inhibition of selectin-mediated interactions during the hematogenous phase of carcinoma metastasis: rationale for clinical studies in humans. Semin. Thromb. Hemost. 28, 53-66 (2002).
32. Vlodavsky, I. et al. Extracellular matrix-resident growth factors and enzymes: possible involvement in tumor metastasis and angiogenesis. Cancer Metastasis Rev. 9, 203-226 (1990).
33. Vlodavsky, I. et al. Mammalian heparanase: involvement in cancer metastasis, angiogenesis and normal development. Sem. Cancer Biol. 12, 121-129 (2002).
34. Parish, C. R., Coombe, D. R., Jakobsen, K. B., Bennett, F. A. & Underwood, P. A. Evidence that sulphated polysaccharides inhibit tumour metastasis by blocking tumour-cell-derived heparanases. Int. J. Cancer 40, 511-518 (1987).
35. Chen, Y. W. et al. Antithrombin regulates matriptase activity involved in plasmin generation, syndecan shedding, and HGF activation in keratinocytes. PLoS One 8, e62826 (2013).
36. Lecumberri, R. et al. Adjuvant therapy with bemoparin in patients with limited stage small cell lung cancer: Results from the ABEL study. Thromb. Res. 132, 660-670 (2013).
37. Liao, W.-Y. et al. Heparin co-factor II enhances cell motility and promotes metastasis in non-small cell lung cancer. J. Pathol. 235, 50-64 (2015).
38. Takeuchi, A. et al. Low molecular weight heparin suppresses receptor for advanced glycation end products-mediated expression of malignant phenotype in human fibrosarcoma cells. Cancer Sci. 104, 740-749 (2013).
39. Friedman, H. S. et al. Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J. Clin. Oncol. 27, 4733-4740 (2009).
40. Sandler, A. et al. Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N. Engl. J. Med. 355, 2542-2550 (2006).
41. Shojaei, F. Anti-Angiogenesis therapy in cancer: current challenges and future perspectives. Cancer Lett. 320, 130-137 (2012).
42. Masters, J. R. et al. Short tandem repeat profiling provides an international reference standard for human cell lines. Proc. Natl. Acad. Sci. USA 98, 8012-8017 (2001).
43. Mushunje, A., Evans, G., Brennan, S. O., Carrell, R. W. & Zhou, A. Latent antithrombin and its detection, formation and turnover in the circulation. J. Thromb. Haemost. 2, 2170-2177 (2004).
44. Bertl, E., Bartsch, H. & Gerhauser, C. Inhibition of angiogenesis and endothelial cell functions are novel sulforaphane-mediated mechanisms in chemoprevention. Mol. Cancer Ther. 5, 575-585 (2006).
45. Martin-Villar, E. et al. Podoplanin mediates ECM degradation by squamous carcinoma cells through control of invadopodia stability. Oncogene 34, 4531-4544 (2015).