Identification of thrombin-like activity in ovarian cancer associated ascites and modulation of multiple cytokine networks

Thrombosis and Haemostasis

Volumn 106, Issue 4, 2011, Pages 705-711

  Naldini, Antonella ^a   Morena, Emilia ^a   Belotti, Dorina ^b   Carraro, Fabio ^a   Allavena, Paola ^c   Giavazzi, Raffaella ^b  

^a UNIVERSITY OF SIENA   (Italy)

^b MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^c HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

Author keywords

Coagulation; Cytokines; Inflammation; Thrombin; Tumour microenvironment

Indexed keywords

ALANYLTYROSYLGLYCYLPROPYLLYSINE; ANTICOAGULANT AGENT; ANTITHROMBIN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; PEPTIDE; PROTEINASE ACTIVATED RECEPTOR; THREONYLPHENYLALANYLLEUCYLLEUCYLARGINYLASPARAGINE; THROMBIN; UNCLASSIFIED DRUG;

ARTICLE; ASCITES; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOMODULATION; MONOCYTE; OVARY CANCER; PRIORITY JOURNAL; PROTEIN FUNCTION; TUMOR GROWTH; TUMOR MICROENVIRONMENT;

ASCITES; ASCITIC FLUID; BLOOD COAGULATION; CARCINOMA; CELLS, CULTURED; CYTOKINES; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE REGULATORY NETWORKS; HUMANS; IMMUNOMODULATION; LEUKOCYTES, MONONUCLEAR; OLIGOPEPTIDES; OVARIAN NEOPLASMS; PARACRINE COMMUNICATION; RECEPTOR, PAR-1; THROMBIN; TUMOR ESCAPE; TUMOR MICROENVIRONMENT;

EID: 80053214214     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1160/TH11-05-0311     Document Type: Article

References (46)

1. Rak J, Yu JL, Luyendyk J, et al. Oncogenes, trousseau syndrome, and cancer-related changes in the coagulome of mice and humans. Cancer Res 2006; 66: 10643-10646.
2. Coussens LM, Werb Z. Inflammation and cancer. Nature 2002; 420: 860-867.
3. Balkwill F, Charles KA, Mantovani A. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 2005; 7: 211-217.
4. Mehrad B, Keane MP, Strieter RM. Chemokines as mediators of angiogenesis. Thromb Haemost 2007; 97: 755-762.
5. Sica A, Saccani A, Bottazzi B, et al. Autocrine production of IL-10 mediates defective IL-12 production and NF-kappa B activation in tumor-associated macrophages. J Immunol 2000; 164: 762-767.
6. Chen D, Dorling A. Critical roles for thrombin in acute and chronic inflammation. J Thromb Haemost 2009; 7 (Suppl 1): 122-126.
7. Coughlin SR, Camerer E. PARticipation in inflammation. J Clin Invest 2003; 111: 25-27.
8. Naldini A, Carney DH, Bocci V, et al. Thrombin enhances T cell proliferative responses and cytokine production. Cell Immunol 1993; 147: 367-377.
9. Colognato R, Slupsky JR, Jendrach M, et al. Differential expression and regulation of protease-activated receptors in human peripheral monocytes and monocytederived antigen-presenting cells. Blood 2003; 102: 2645-2652.
10. Colotta F, Sciacca FL, Sironi M, et al. Expression of monocyte chemotactic protein-1 by monocytes and endothelial cells exposed to thrombin. Amer J Pathol 1994; 144: 975-985.
11. Bar-Shavit R, Kahn A, Fenton JWI, et al. Chemotactic response of monocytes to thrombin. J Cell Biol 1983; 96: 282-285.
12. Tsopanoglou NE, Maragoudakis ME. Role of thrombin in angiogenesis and tumor progression. Semin Thromb Hemost 2004; 30: 63-69.
13. Nierodzik ML, Karpatkin S. Thrombin induces tumor growth, metastasis, and angiogenesis: Evidence for a thrombin-regulated dormant tumor phenotype. Cancer Cell 2006; 10: 355-362.
14. Silini A, Ghilardi C, Ardinghi C, et al. Protease-activated receptor-1 (PAR-1) promotes the motility of human melanomas and is associated to their metastatic phenotype. Clin Exp Metastasis 2010; 27: 43-53.
15. Zacharski LR, Wojtukiewicz MZ, Costantini V, et al. Pathways of coagulation/fibrinolysis activation in malignancy. Semin Thromb Hemost 1992; 18: 104-116.
16. Grisaru-Granovsky S, Salah Z, Maoz M, et al. Differential expression of protease activated receptor 1 (Par1) and pY397FAK in benign and malignant human ovarian tissue samples. Int J Cancer 2005; 113: 372-378.
17. Wang X, Wang E, Kavanagh JJ, et al. Ovarian cancer, the coagulation pathway, and inflammation. J Transl Med 2005; 3: 25.
18. Cannistra SA. Cancer of the ovary. N Engl J Med 2004; 351: 2519-2529.
19. Giuntoli RL, Webb TJ, Zoso A, et al. Ovarian cancer-associated ascites demonstrates altered immune environment: implications for antitumor immunity. Anticancer Res 2009; 29: 2875-2884.
20. Naldini A, Aarden L, Pucci A, et al. Inhibition of interleukin-12 expression by {alpha}-thrombin in human peripheral blood mononuclear cells: a potential mechanism for modulating Th1/Th2 responses. Br J Pharmacol 2003; 140: 980-986.
21. Naldini A, Bernini C, Pucci A, et al. Thrombin-mediated IL-10 up-regulation involves protease-activated receptor (PAR)-1 expression in human mononuclear leukocytes. J Leukoc Biol 2005; 78: 736-744.
22. Spentzos D, Levine DA, Ramoni MF, et al. Gene expression signature with independent prognostic significance in epithelial ovarian cancer. J Clin Oncol 2004; 22: 4700-4710.
23. Schutyser E, Struyf S, Proost P, et al. Identification of biologically active chemokine isoforms from ascitic fluid and elevated levels of CCL18/pulmonary and activation- regulated chemokine in ovarian carcinoma. J Biol Chem 2002; 277: 24584-24593.
24. Ramjee MK. The use of fluorogenic substrates to monitor thrombin generation for the analysis of plasma and whole blood coagulation. Anal Biochem 2000; 277: 11-18.
25. Butenas S, van't Veer C, Mann KG. Normal thrombin generation. Blood 1999; 94: 2169-2178.
26. Naldini A, Leali D, Pucci A, et al. Cutting edge: IL-1beta mediates the proangiogenic activity of osteopontin-activated human monocytes. J Immunol 2006; 177: 4267-4270.
27. Peri G, Milanese C, Matteucci C, et al. A new monoclonal antibody (5D3-F7) which recognizes human monocyte-chemotactic protein-1 but not related chemokines. Development of a sandwich ELISA and in situ detection of producing cells. J Immunol Methods 1994; 174: 249-257.
28. Vandesompele J, De PK, Pattyn F, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002; 3: 1-12.
29. Fenton II JW. Thrombin. Ann N Y Acad Sci 1986; 485: 5-15.
30. Gieseler F, Luhr I, Kunze T, et al. Activated coagulation factors in human malignant effusions and their contribution to cancer cell metastasis and therapy. Thromb Haemost 2007; 97: 1023-1030.
31. Delvaeye M, Conway EM. Coagulation and innate immune responses: can we view them separately? Blood 2009; 114: 2367-2374.
32. Johnson K, Aarden L, Choi Y, et al. The proinflammatory cytokine response to coagulation and endotoxin in whole blood. Blood 1996; 87: 5051-5060.
33. Loercher AE, Nash MA, Kavanagh JJ, et al. Identification of an IL-10-producing HLA-DR-negative monocyte subset in the malignant ascites of patients with ovarian carcinoma that inhibits cytokine protein expression and proliferation of autologous T cells. J Immunol 1999; 163: 6251-6260.
34. Naldini A, Morena E, Filippi I, et al. Thrombin inhibits IFN-gamma production in human peripheral blood mononuclear cells by promoting a Th2 profile. J Interferon Cytokine Res 2006; 26: 793-799.
35. Yin YJ, Salah Z, Grisaru-Granovsky S, et al. Human protease-activated receptor 1 expression in malignant epithelia: a role in invasiveness. Arterioscler Thromb Vasc Biol 2003; 23: 940-944.
36. VanDeWater L, Tracy PB, Aronson D, et al. Tumor cell generation of thrombin via functional prothrombinase assembly. Cancer Res 1985; 45: 5521-5525.
37. Palumbo JS. Mechanisms linking tumor cell-associated procoagulant function to tumor dissemination. Semin Thromb Hemost 2008; 34: 154-160.
38. Traby L, Kaider A, Schmid R, et al. The effects of low-molecular-weight heparin at two different dosages on thrombin generation in cancer patients. A randomised controlled trial. Thromb Haemost 2010; 104: 92-99.
39. Nieman MT, LaRusch G, Fang C, et al. Oral thrombostatin FM19 inhibits prostate cancer. Thromb Haemost 2010; 104: 1044-1048.
40. Chopra V, V, Dinh TV, Hannigan EV. Angiogenin, Interleukins, and Growth-Factor Levels in Serum of Patients with Ovarian Cancer: Correlation with Angiogenesis. Cancer J Sci Am 1996; 2: 279.
41. Manenti L, Paganoni P, Floriani I, et al. Expression levels of vascular endothelial growth factor, matrix metalloproteinases 2 and 9 and tissue inhibitor of metalloproteinases 1 and 2 in the plasma of patients with ovarian carcinoma. Eur J Cancer 2003; 39: 1948-1956.
42. Duluc D, Delneste Y, Tan F, et al. Tumor-associated leukemia inhibitory factor and IL-6 skew monocyte differentiation into tumor-associated macrophage-like cells. Blood 2007; 110: 4319-4330.
43. Salah Z, Maoz M, Pokroy E, et al. Protease-activated receptor-1 (hPar1), a survival factor eliciting tumor progression. Mol Cancer Res 2007; 5: 229-240.
44. Naldini A, Filippi I, Ardinghi C, et al. Identification of a functional role for the protease-activated receptor-1 in hypoxic breast cancer cells. Eur J Cancer 2009; 45: 454-460.
45. Sica A, Saccani A, Bottazzi B, et al. Defective expression of the monocyte chemotactic protein-1 receptor CCR2 in macrophages associated with human ovarian carcinoma. J Immunol 2000; 164: 733-738.
46. Niers TM, Bruggemann LW, Klerk CP, et al. Differential effects of anticoagulants on tumor development of mouse cancer cell lines B16, K1735 and CT26 in lung. Clin Exp Metastasis 2009; 26: 171-178.