Ascidian dermatan sulfates attenuate metastasis, inflammation and thrombosis by inhibition of P-selectin

Journal of Thrombosis and Haemostasis

Volumn 9, Issue 9, 2011, Pages 1807-1815

  Kozlowski, E O ^a,b   Pavao, M S G ^b   Borsig, L ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Dermatan sulfate; Inflammation; Metastasis; Thrombosis

Indexed keywords

DERMATAN SULFATE; DISACCHARIDE; GLYCOSAMINOGLYCAN; HEPARIN; HEPARIN COFACTOR II; PADGEM PROTEIN; THIOGLYCOLIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY THROMBOSIS; ARTICLE; ASCIDIACEA; BIOLOGICAL ACTIVITY; CANCER CELL; CELL INFILTRATION; COLON CARCINOMA; COMPETITIVE INHIBITION; CONTROLLED STUDY; EXPERIMENTAL MODEL; HUMAN; HUMAN CELL; INFLAMMATORY CELL; MELANOMA; METASTASIS; MOUSE; NONHUMAN; PARTIAL THROMBOPLASTIN TIME; PERITONITIS; PHALLUSIA NIGRA; PRIORITY JOURNAL; STRUCTURE ANALYSIS; STYELA PLICATA; SULFATION; THROMBOCYTE ACTIVATION; THROMBOGENESIS;

ANIMALS; CELL LINE, TUMOR; COLONIC NEOPLASMS; DERMATAN SULFATE; HUMANS; INFLAMMATION; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOPLASM METASTASIS; NEOPLASMS, EXPERIMENTAL; NEUTROPHILS; P-SELECTIN; THROMBOSIS; UROCHORDATA;

EID: 80052401501     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2011.04401.x     Document Type: Article

References (47)

1. Varki A. Trousseau's syndrome: multiple definitions and multiple mechanisms. Blood 2007; 110: 1723-9.
2. Rickles FR. Mechanisms of cancer-induced thrombosis in cancer. Pathophysiol Haemost Thromb 2006; 35: 103-10.
3. Karpatkin S, Pearlstein E, Ambrogio C, Coller BS. Role of adhesive proteins in platelet tumor interaction in vitro and metastasis formation in vivo. J Clin Invest 1988; 81: 1012-19.
4. Borsig L, Wong R, Feramisco J, Nadeau DR, Varki NM, Varki A. Heparin and cancer revisited: mechanistic connections involving platelets, P-selectin, carcinoma mucins, and tumor metastasis. Proc Natl Acad Sci USA 2001; 98: 3352-7.
5. Ho-Tin-Noe B, Goerge T, Cifuni SM, Duerschmied D, Wagner DD. Platelet granule secretion continuously prevents intratumor hemorrhage. Cancer Res 2008; 68: 6851-8.
6. Frenette PS, Moyna C, Hartwell DW, Lowe JB, Hynes RO, Wagner DD. Platelet-endothelial interactions in inflamed mesenteric venules. Blood 1998; 91: 1318-24.
7. Italiano JE Jr, Richardson JL, Patel-Hett S, Battinelli E, Zaslavsky A, Short S, Ryeom S, Folkman J, Klement GL. Angiogenesis is regulated by a novel mechanism: pro- and antiangiogenic proteins are organized into separate platelet alpha granules and differentially released. Blood 2008; 111: 1227-33.
8. Goerge T, Ho-Tin-Noe B, Carbo C, Benarafa C, Remold-O'Donnell E, Zhao BQ, Cifuni SM, Wagner DD. Inflammation induces hemorrhage in thrombocytopenia. Blood 2008; 111: 4958-64.
9. Ludwig RJ, Schon MP, Boehncke WH. P-selectin: a common therapeutic target for cardiovascular disorders, inflammation and tumour metastasis. Expert Opin Ther Targets 2007; 11: 1103-17.
10. Polgar J, Matuskova J, Wagner DD. The P-selectin, tissue factor, coagulation triad. J Thromb Haemost 2005; 3: 1590-6.
11. Läubli H, Borsig L. Selectins promote tumor metastasis. Semin Cancer Biol 2010; 20: 169-77.
12. Kansas GS. Selectins and their ligands: current concepts and controversies. Blood 1996; 88: 3259-87.
13. Borsig L, Wong R, Hynes RO, Varki NM, Varki A. Synergistic effects of L- and P-selectin in facilitating tumor metastasis can involve non-mucin ligands and implicate leukocytes as enhancers of metastasis. Proc Natl Acad Sci USA 2002; 99: 2193-8.
14. Ludwig RJ, Boehme B, Podda M, Henschler R, Jager E, Tandi C, Boehncke WH, Zollner TM, Kaufmann R, Gille J. Endothelial P-selectin as a target of heparin action in experimental melanoma lung metastasis. Cancer Res 2004; 64: 2743-50.
15. Nieswandt B, Hafner M, Echtenacher B, Mannel DN. Lysis of tumor cells by natural killer cells in mice is impeded by platelets. Cancer Res 1999; 59: 1295-300.
16. Connolly GC, Khorana AA. Emerging risk stratification approaches to cancer-associated thrombosis: risk factors, biomarkers and a risk score. Thromb Res 2010; 125(Suppl. 2): S1-7.
17. Sierko E, Wojtukiewicz MZ. Platelets and angiogenesis in malignancy. Semin Thromb Hemost 2004; 30: 95-108.
18. Thomas GM, Panicot-Dubois L, Lacroix R, Dignat-George F, Lombardo D, Dubois C. Cancer cell-derived microparticles bearing P-selectin glycoprotein ligand 1 accelerate thrombus formation in vivo. J Exp Med 2009; 206: 1913-27.
19. Myers DD Jr, Rectenwald JE, Bedard PW, Kaila N, Shaw GD, Schaub RG, Farris DM, Hawley AE, Wrobleski SK, Henke PK, Wakefield TW. Decreased venous thrombosis with an oral inhibitor of P selectin. J Vasc Surg 2005; 42: 329-36.
20. Falanga A, Marchetti M. Heparin in tumor progression and metastatic dissemination. Semin Thromb Hemost 2007; 33: 688-94.
21. Zacharski LR, Loynes JT. Low-molecular-weight heparin in oncology. Anticancer Res 2003; 23: 2789-93.
22. Kuderer NM, Ortel TL, Francis CW. Impact of venous thromboembolism and anticoagulation on cancer and cancer survival. J Clin Oncol 2009; 27: 4902-11.
23. Mousa SA, Petersen LJ. Anti-cancer properties of low-molecular-weight heparin: preclinical evidence. Thromb Haemost 2009; 102: 258-67.
24. Borsig L, Stevenson JL, Varki A. Heparin in cancer: role of selectin interactions. In: Khorana AA, Francis CW, eds. Cancer-associated Thrombosis. New York: Informa Healthcare, 2007: 97-113.
25. Hostettler N, Naggi A, Torri G, Casu B, Vlodavsky I, Borsig L. P-selectin- and heparanase-dependent antimetastatic activity of non-anticoagulant heparins. FASEB J 2007; 21: 3562-72.
26. Kragh M, Binderup L, Vig Hjarnaa PJ, Bramm E, Johansen KB, Frimundt Petersen C. Non-anti-coagulant heparin inhibits metastasis but not primary tumor growth. Oncol Rep 2005; 14: 99-104.
27. Pavao MS, Aiello KR, Werneck CC, Silva LC, Valente AP, Mulloy B, Colwell NS, Tollefsen DM, Mourao PA. Highly sulfated dermatan sulfates from Ascidians. Structure versus anticoagulant activity of these glycosaminoglycans. J Biol Chem 1998; 273: 27848-57.
28. Gigli M, Ghiselli G, Torri G, Naggi A, Rizzo V. A comparative study of low-density lipoprotein interaction with glycosaminoglycans. Biochim Biophys Acta 1993; 1167: 211-17.
29. Läubli H, Spanaus KS, Borsig L. Selectin-mediated activation of endothelial cells induces expression of CCL5 and promotes metastasis through recruitment of monocytes. Blood 2009; 114: 4583-91.
30. Kurz KD, Main BW, Sandusky GE. Rat model of arterial thrombosis induced by ferric chloride. Thromb Res 1990; 60: 269-80.
31. Koenig A, Norgard-Sumnicht K, Linhardt R, Varki A. Differential interactions of heparin and heparan sulfate glycosaminoglycans with the selectins. Implications for the use of unfractionated and low molecular weight heparins as therapeutic agents. J Clin Invest 1998; 101: 877-89.
32. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008; 454: 436-44.
33. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell 2010; 140: 883-99.
34. Ay C, Simanek R, Vormittag R, Dunkler D, Alguel G, Koder S, Kornek G, Marosi C, Wagner O, Zielinski C, Pabinger I. High plasma levels of soluble P-selectin are predictive of venous thromboembolism in cancer patients: results from the Vienna Cancer and Thrombosis Study (CATS). Blood 2008; 112: 2703-8.
35. Rectenwald JE, Myers DD Jr, Hawley AE, Longo C, Henke PK, Guire KE, Schmaier AH, Wakefield TW. D-dimer, P-selectin, and microparticles: novel markers to predict deep venous thrombosis. A pilot study. Thromb Haemost 2005; 94: 1312-17.
36. Ramacciotti E, Hawley AE, Farris DM, Ballard NE, Wrobleski SK, Myers DD Jr, Henke PK, Wakefield TW. Leukocyte- and platelet-derived microparticles correlate with thrombus weight and tissue factor activity in an experimental mouse model of venous thrombosis. Thromb Haemost 2009; 101: 748-54.
37. Vicente CP, He L, Pavao MS, Tollefsen DM. Antithrombotic activity of dermatan sulfate in heparin cofactor II-deficient mice. Blood 2004; 104: 3965-70.
38. Vicente CP, Zancan P, Peixoto LL, Alves-Sa R, Araujo FS, Mourao PA, Pavao MS. Unbalanced effects of dermatan sulfates with different sulfation patterns on coagulation, thrombosis and bleeding. Thromb Haemost 2001; 86: 1215-20.
39. Yokoyama S, Ikeda H, Haramaki N, Yasukawa H, Murohara T, Imaizumi T. Platelet P-selectin plays an important role in arterial thrombogenesis by forming large stable platelet-leukocyte aggregates. J Am Coll Cardiol 2005; 45: 1280-6.
40. Palabrica T, Lobb R, Furie BC, Aronovitz M, Benjamin C, Hsu YM, Sajer SA, Furie B. Leukocyte accumulation promoting fibrin deposition is mediated in vivo by P-selectin on adherent platelets. Nature 1992; 359: 848-51.
41. Hrachovinova I, Cambien B, Hafezi-Moghadam A, Kappelmayer J, Camphausen RT, Widom A, Xia L, Kazazian HH Jr, Schaub RG, McEver RP, Wagner DD. Interaction of P-selectin and PSGL-1 generates microparticles that correct hemostasis in a mouse model of hemophilia A. Nat Med 2003; 9: 1020-5.
42. Falati S, Liu Q, Gross P, Merrill-Skoloff G, Chou J, Vandendries E, Celi A, Croce K, Furie BC, Furie B. Accumulation of tissue factor into developing thrombi in vivo is dependent upon microparticle P-selectin glycoprotein ligand 1 and platelet P-selectin. J Exp Med 2003; 197: 1585-98.
43. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 2007; 7: 678-89.
44. Mulloy B. The specificity of interactions between proteins and sulfated polysaccharides. An Acad Bras Cienc 2005; 77: 651-64.
45. Geng JG, Chen M, Chou KC. P-selectin cell adhesion molecule in inflammation, thrombosis, cancer growth and metastasis. Curr Med Chem 2004; 11: 2153-60.
46. Ludwig RJ, Alban S, Bistrian R, Boehncke WH, Kaufmann R, Henschler R, Gille J. The ability of different forms of heparins to suppress P-selectin function in vitro correlates to their inhibitory capacity on bloodborne metastasis in vivo. Thromb Haemost 2006; 95: 535-40.
47. Wang L, Brown JR, Varki A, Esko JD. Heparin's anti-inflammatory effects require glucosamine 6-O-sulfation and are mediated by blockade of L- and P-selectins. J Clin Invest 2002; 110: 127-36.