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Published in: Breast Cancer Research 4/2013

01-08-2013 | Review

Platelets, coagulation and fibrinolysis in breast cancer progression

Authors: Inder Lal, Kim Dittus, Chris E Holmes

Published in: Breast Cancer Research | Issue 4/2013

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Abstract

The progression of breast cancer from early-stage to metastatic disease results from a series of events during which malignant cells invade and travel within the bloodstream to distant sites, leading to a clonogenic accumulation of tumor cells in non-breast tissue. While mechanistically complex, an emerging literature supports hemostatic elements as an important patient factor that facilitates the metastatic potential of breast cancer. Hemostatic elements involved include platelets, coagulation, and fibrinolysis. Key steps in breast tumor progression, including cellular transformation, proliferation, tumor cell survival, and angiogenesis, can be mediated by components of the hemostatic system. Thus, the hemostatic system provides potential targets for novel therapeutic approaches to breast cancer therapy with drugs in current use and in development. The present article provides a comprehensive overview of the evidence and mechanisms supporting the roles played by platelets, coagulation activation, and the fibrinolytic system in breast cancer progression.
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Literature
1.
go back to reference Hanahan D, Weinberg RA: Hallmarks of cancer: the next generation. Cell. 2011, 144: 646-674. 10.1016/j.cell.2011.02.013.CrossRefPubMed Hanahan D, Weinberg RA: Hallmarks of cancer: the next generation. Cell. 2011, 144: 646-674. 10.1016/j.cell.2011.02.013.CrossRefPubMed
2.
go back to reference Chew HK, Wun T, Harvey DJ, Zhou H, White RH: Incidence of venous thromboembolism and the impact on survival in breast cancer patients. J Clin Oncol. 2007, 25: 70-76.CrossRefPubMed Chew HK, Wun T, Harvey DJ, Zhou H, White RH: Incidence of venous thromboembolism and the impact on survival in breast cancer patients. J Clin Oncol. 2007, 25: 70-76.CrossRefPubMed
3.
go back to reference Caine GJ, Stonelake PS, Rea D, Lip GY: Coagulopathic complications in breast cancer. Cancer. 2003, 98: 1578-1586. 10.1002/cncr.11702.CrossRefPubMed Caine GJ, Stonelake PS, Rea D, Lip GY: Coagulopathic complications in breast cancer. Cancer. 2003, 98: 1578-1586. 10.1002/cncr.11702.CrossRefPubMed
4.
go back to reference Caine GJ, Lip GY, Stonelake PS, Ryan P, Blann AD: Platelet activation, coagulation and angiogenesis in breast and prostate carcinoma. Thromb Haemost. 2004, 92: 185-190.PubMed Caine GJ, Lip GY, Stonelake PS, Ryan P, Blann AD: Platelet activation, coagulation and angiogenesis in breast and prostate carcinoma. Thromb Haemost. 2004, 92: 185-190.PubMed
5.
go back to reference Ferriere JP, Bernard D, Legros M, Chassagne J, Chollet P, Gaillard G, Plagne R: beta-Thromboglobulin in patients with breast cancer. Am J Hematol. 1985, 19: 47-53. 10.1002/ajh.2830190107.CrossRefPubMed Ferriere JP, Bernard D, Legros M, Chassagne J, Chollet P, Gaillard G, Plagne R: beta-Thromboglobulin in patients with breast cancer. Am J Hematol. 1985, 19: 47-53. 10.1002/ajh.2830190107.CrossRefPubMed
6.
go back to reference Alonso-Escolano D, Strongin AY, Chung AW, Deryugina EI, Radomski MW: Membrane type-1 matrix metalloproteinase stimulates tumour cell-induced platelet aggregation: role of receptor glycoproteins. Br J Pharmacol. 2004, 141: 241-252. 10.1038/sj.bjp.0705606.CrossRefPubMed Alonso-Escolano D, Strongin AY, Chung AW, Deryugina EI, Radomski MW: Membrane type-1 matrix metalloproteinase stimulates tumour cell-induced platelet aggregation: role of receptor glycoproteins. Br J Pharmacol. 2004, 141: 241-252. 10.1038/sj.bjp.0705606.CrossRefPubMed
7.
go back to reference Taucher S, Salat A, Gnant M, Kwasny W, Mlineritsch B, Menzel RC, Schmid M, Smola MG, Stierer M, Tausch C, Galid A, Steger G, Jakesz R, Austrian Breast and Colorectal Cancer Study Group: Impact of pretreatment thrombocytosis on survival in primary breast cancer. Thromb Haemost. 2003, 89: 1098-1106.PubMed Taucher S, Salat A, Gnant M, Kwasny W, Mlineritsch B, Menzel RC, Schmid M, Smola MG, Stierer M, Tausch C, Galid A, Steger G, Jakesz R, Austrian Breast and Colorectal Cancer Study Group: Impact of pretreatment thrombocytosis on survival in primary breast cancer. Thromb Haemost. 2003, 89: 1098-1106.PubMed
8.
go back to reference Sierko E, Wojtukiewicz MZ: Platelets and angiogenesis in malignancy. Semin Thromb Hemost. 2004, 30: 95-108.CrossRefPubMed Sierko E, Wojtukiewicz MZ: Platelets and angiogenesis in malignancy. Semin Thromb Hemost. 2004, 30: 95-108.CrossRefPubMed
9.
go back to reference Bambace NM, Holmes CE: The platelet contribution to cancer progression. J Thromb Haemost. 2011, 9: 237-249. 10.1111/j.1538-7836.2010.04131.x.CrossRefPubMed Bambace NM, Holmes CE: The platelet contribution to cancer progression. J Thromb Haemost. 2011, 9: 237-249. 10.1111/j.1538-7836.2010.04131.x.CrossRefPubMed
10.
go back to reference Nurden AT: Platelets, inflammation and tissue regeneration. Thromb Haemost. 2011, 105 (Suppl 1): S13-33.CrossRefPubMed Nurden AT: Platelets, inflammation and tissue regeneration. Thromb Haemost. 2011, 105 (Suppl 1): S13-33.CrossRefPubMed
11.
go back to reference Gasic GJ, Gasic TB, Stewart CC: Antimetastatic effects associated with platelet reduction. Proc Natl Acad Sci USA. 1968, 61: 46-52. 10.1073/pnas.61.1.46.CrossRefPubMedPubMedCentral Gasic GJ, Gasic TB, Stewart CC: Antimetastatic effects associated with platelet reduction. Proc Natl Acad Sci USA. 1968, 61: 46-52. 10.1073/pnas.61.1.46.CrossRefPubMedPubMedCentral
12.
go back to reference Placke T, Orgel M, Schaller M, Jung G, Rammensee HG, Kopp HG, Salih HR: Platelet-derived MHC class I confers a pseudonormal phenotype to cancer cells that subverts the antitumor reactivity of natural killer immune cells. Cancer Res. 2012, 72: 440-448. 10.1158/0008-5472.CAN-11-1872.CrossRefPubMed Placke T, Orgel M, Schaller M, Jung G, Rammensee HG, Kopp HG, Salih HR: Platelet-derived MHC class I confers a pseudonormal phenotype to cancer cells that subverts the antitumor reactivity of natural killer immune cells. Cancer Res. 2012, 72: 440-448. 10.1158/0008-5472.CAN-11-1872.CrossRefPubMed
13.
go back to reference Karpatkin S, Ambrogio C, Pearlstein E: The role of tumor-induced platelet aggregation, platelet adhesion and adhesive proteins in tumor metastasis. Prog Clin Biol Res. 1988, 283: 585-606.PubMed Karpatkin S, Ambrogio C, Pearlstein E: The role of tumor-induced platelet aggregation, platelet adhesion and adhesive proteins in tumor metastasis. Prog Clin Biol Res. 1988, 283: 585-606.PubMed
14.
go back to reference Labelle M, Begum S, Hynes RO: Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer Cell. 2011, 20: 576-590. 10.1016/j.ccr.2011.09.009.CrossRefPubMedPubMedCentral Labelle M, Begum S, Hynes RO: Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer Cell. 2011, 20: 576-590. 10.1016/j.ccr.2011.09.009.CrossRefPubMedPubMedCentral
15.
go back to reference Boucharaba A, Guillet B, Menaa F, Hneino M, van Wijnen AJ, Clezardin P, Peyruchaud O: Bioactive lipids lysophosphatidic acid and sphingosine 1-phosphate mediate breast cancer cell biological functions through distinct mechanisms. Oncol Res. 2009, 18: 173-184. 10.3727/096504009790217399.CrossRefPubMed Boucharaba A, Guillet B, Menaa F, Hneino M, van Wijnen AJ, Clezardin P, Peyruchaud O: Bioactive lipids lysophosphatidic acid and sphingosine 1-phosphate mediate breast cancer cell biological functions through distinct mechanisms. Oncol Res. 2009, 18: 173-184. 10.3727/096504009790217399.CrossRefPubMed
16.
go back to reference Caine GJ, Lip GY, Blann AD: Platelet-derived VEGF, Flt-1, angiopoietin-1 and P-selectin in breast and prostate cancer: further evidence for a role of platelets in tumour angiogenesis. Ann Med. 2004, 36: 273-277. 10.1080/07853890410026098.CrossRefPubMed Caine GJ, Lip GY, Blann AD: Platelet-derived VEGF, Flt-1, angiopoietin-1 and P-selectin in breast and prostate cancer: further evidence for a role of platelets in tumour angiogenesis. Ann Med. 2004, 36: 273-277. 10.1080/07853890410026098.CrossRefPubMed
17.
go back to reference Kuznetsov HS, Marsh T, Markens BA, Castaño Z, Greene-Colozzi A, Hay SA, Brown VE, Richardson AL, Signoretti S, Battinelli EM, McAllister SS: Identification of luminal breast cancers that establish a tumor-supportive macroenvironment defined by proangiogenic platelets and bone marrow-derived cells. Cancer Discov. 2012, 2: 1150-1165. 10.1158/2159-8290.CD-12-0216.CrossRefPubMedPubMedCentral Kuznetsov HS, Marsh T, Markens BA, Castaño Z, Greene-Colozzi A, Hay SA, Brown VE, Richardson AL, Signoretti S, Battinelli EM, McAllister SS: Identification of luminal breast cancers that establish a tumor-supportive macroenvironment defined by proangiogenic platelets and bone marrow-derived cells. Cancer Discov. 2012, 2: 1150-1165. 10.1158/2159-8290.CD-12-0216.CrossRefPubMedPubMedCentral
18.
go back to reference Alonso-Escolano D, Medina C, Cieslik K, Radomski A, Jurasz P, Santos-Martinez MJ, Jiffar T, Ruvolo P, Radomski MW: Protein kinase C delta mediates platelet-induced breast cancer cell invasion. J Pharmacol Exp Ther. 2006, 318: 373-380. 10.1124/jpet.106.103358.CrossRefPubMed Alonso-Escolano D, Medina C, Cieslik K, Radomski A, Jurasz P, Santos-Martinez MJ, Jiffar T, Ruvolo P, Radomski MW: Protein kinase C delta mediates platelet-induced breast cancer cell invasion. J Pharmacol Exp Ther. 2006, 318: 373-380. 10.1124/jpet.106.103358.CrossRefPubMed
19.
go back to reference Oleksowicz L, Mrowiec Z, Schwartz E, Khorshidi M, Dutcher JP, Puszkin E: Characterization of tumor-induced platelet aggregation: the role of immunorelated GPIb and GPIIb/IIIa expression by MCF-7 breast cancer cells. Thromb Res. 1995, 79: 261-274. 10.1016/0049-3848(95)00113-6.CrossRefPubMed Oleksowicz L, Mrowiec Z, Schwartz E, Khorshidi M, Dutcher JP, Puszkin E: Characterization of tumor-induced platelet aggregation: the role of immunorelated GPIb and GPIIb/IIIa expression by MCF-7 breast cancer cells. Thromb Res. 1995, 79: 261-274. 10.1016/0049-3848(95)00113-6.CrossRefPubMed
20.
go back to reference Pacchiarini L, Zucchella M, Milanesi G, Tacconi F, Bonomi E, Canevari A, Grignani G: Thromboxane production by platelets during tumor cell-induced platelet activation. Invasion Metastasis. 1991, 11: 102-109.PubMed Pacchiarini L, Zucchella M, Milanesi G, Tacconi F, Bonomi E, Canevari A, Grignani G: Thromboxane production by platelets during tumor cell-induced platelet activation. Invasion Metastasis. 1991, 11: 102-109.PubMed
21.
go back to reference Grignani G, Pacchiarini L, Ricetti MM, Dionigi P, Jemos V, Zucchella M, Fratino P: Mechanisms of platelet activation by cultured human cancer cells and cells freshly isolated from tumor tissues. Invasion Metastasis. 1989, 9: 298-309.PubMed Grignani G, Pacchiarini L, Ricetti MM, Dionigi P, Jemos V, Zucchella M, Fratino P: Mechanisms of platelet activation by cultured human cancer cells and cells freshly isolated from tumor tissues. Invasion Metastasis. 1989, 9: 298-309.PubMed
22.
go back to reference Felding-Habermann B, O'Toole TE, Smith JW, Fransvea E, Ruggeri ZM, Ginsberg MH, Hughes PE, Pampori N, Shattil SJ, Saven A, Mueller BM: Integrin activation controls metastasis in human breast cancer. Proc Natl Acad Sci USA. 2001, 98: 1853-1858. 10.1073/pnas.98.4.1853.CrossRefPubMedPubMedCentral Felding-Habermann B, O'Toole TE, Smith JW, Fransvea E, Ruggeri ZM, Ginsberg MH, Hughes PE, Pampori N, Shattil SJ, Saven A, Mueller BM: Integrin activation controls metastasis in human breast cancer. Proc Natl Acad Sci USA. 2001, 98: 1853-1858. 10.1073/pnas.98.4.1853.CrossRefPubMedPubMedCentral
23.
go back to reference Battinelli EM, Markens BA, Italiano JE: Release of angiogenesis regulatory proteins from platelet alpha granules: modulation of physiologic and pathologic angiogenesis. Blood. 2011, 118: 1359-1369. 10.1182/blood-2011-02-334524.CrossRefPubMedPubMedCentral Battinelli EM, Markens BA, Italiano JE: Release of angiogenesis regulatory proteins from platelet alpha granules: modulation of physiologic and pathologic angiogenesis. Blood. 2011, 118: 1359-1369. 10.1182/blood-2011-02-334524.CrossRefPubMedPubMedCentral
24.
go back to reference Tokyol C, Ersoz G, Dilek FH, Gencer E, Kosar MN, Dilek ON: Thrombospondin 1 expression and angiogenesis in breast carcinoma and their relation with platelet activity. Ups J Med Sci. 2009, 114: 108-115. 10.1080/03009730902761797.CrossRefPubMedPubMedCentral Tokyol C, Ersoz G, Dilek FH, Gencer E, Kosar MN, Dilek ON: Thrombospondin 1 expression and angiogenesis in breast carcinoma and their relation with platelet activity. Ups J Med Sci. 2009, 114: 108-115. 10.1080/03009730902761797.CrossRefPubMedPubMedCentral
25.
go back to reference Janowska-Wieczorek A, Marquez-Curtis LA, Wysoczynski M, Ratajczak MZ: Enhancing effect of platelet-derived microvesicles on the invasive potential of breast cancer cells. Transfusion. 2006, 46: 1199-1209. 10.1111/j.1537-2995.2006.00871.x.CrossRefPubMed Janowska-Wieczorek A, Marquez-Curtis LA, Wysoczynski M, Ratajczak MZ: Enhancing effect of platelet-derived microvesicles on the invasive potential of breast cancer cells. Transfusion. 2006, 46: 1199-1209. 10.1111/j.1537-2995.2006.00871.x.CrossRefPubMed
26.
go back to reference Kopp HG, Placke T, Salih HR: Platelet-derived transforming growth factor-beta down-regulates NKG2D thereby inhibiting natural killer cell antitumor reactivity. Cancer Res. 2009, 69: 7775-7783. 10.1158/0008-5472.CAN-09-2123.CrossRefPubMed Kopp HG, Placke T, Salih HR: Platelet-derived transforming growth factor-beta down-regulates NKG2D thereby inhibiting natural killer cell antitumor reactivity. Cancer Res. 2009, 69: 7775-7783. 10.1158/0008-5472.CAN-09-2123.CrossRefPubMed
27.
go back to reference Drabsch Y, ten Dijke P: TGF-beta signaling in breast cancer cell invasion and bone metastasis. J Mammary Gland Biol Neoplasia. 2011, 16: 97-108. 10.1007/s10911-011-9217-1.CrossRefPubMedPubMedCentral Drabsch Y, ten Dijke P: TGF-beta signaling in breast cancer cell invasion and bone metastasis. J Mammary Gland Biol Neoplasia. 2011, 16: 97-108. 10.1007/s10911-011-9217-1.CrossRefPubMedPubMedCentral
28.
go back to reference Coupland LA, Chong BH, Parish CR: Platelets and P-selectin control tumor cell metastasis in an organ-specific manner and independently of NK cells. Cancer Res. 2012, 72: 4662-4671. 10.1158/0008-5472.CAN-11-4010.CrossRefPubMed Coupland LA, Chong BH, Parish CR: Platelets and P-selectin control tumor cell metastasis in an organ-specific manner and independently of NK cells. Cancer Res. 2012, 72: 4662-4671. 10.1158/0008-5472.CAN-11-4010.CrossRefPubMed
29.
go back to reference Stubke K, Wicklein D, Herich L, Schumacher U, Nehmann N: Selectin-deficiency reduces the number of spontaneous metastases in a xenograft model of human breast cancer. Cancer Lett. 2012, 321: 89-99. 10.1016/j.canlet.2012.02.019.CrossRefPubMed Stubke K, Wicklein D, Herich L, Schumacher U, Nehmann N: Selectin-deficiency reduces the number of spontaneous metastases in a xenograft model of human breast cancer. Cancer Lett. 2012, 321: 89-99. 10.1016/j.canlet.2012.02.019.CrossRefPubMed
30.
go back to reference Mazouni C, Arun B, Andre F, Ayers M, Krishnamurthy S, Wang B, Hortobagyi GN, Buzdar AU, Pusztai L: Collagen IV levels are elevated in the serum of patients with primary breast cancer compared to healthy volunteers. Br J Cancer. 2008, 99: 68-71. 10.1038/sj.bjc.6604443.CrossRefPubMedPubMedCentral Mazouni C, Arun B, Andre F, Ayers M, Krishnamurthy S, Wang B, Hortobagyi GN, Buzdar AU, Pusztai L: Collagen IV levels are elevated in the serum of patients with primary breast cancer compared to healthy volunteers. Br J Cancer. 2008, 99: 68-71. 10.1038/sj.bjc.6604443.CrossRefPubMedPubMedCentral
31.
go back to reference Brooks SA, Lomax-Browne HJ, Carter TM, Kinch CE, Hall DM: Molecular interactions in cancer cell metastasis. Acta Histochem. 2010, 112: 3-25. 10.1016/j.acthis.2008.11.022.CrossRefPubMed Brooks SA, Lomax-Browne HJ, Carter TM, Kinch CE, Hall DM: Molecular interactions in cancer cell metastasis. Acta Histochem. 2010, 112: 3-25. 10.1016/j.acthis.2008.11.022.CrossRefPubMed
32.
go back to reference Cooney CA, Jousheghany F, Yao-Borengasser A, Phanavanh B, Gomes T, Kieber-Emmons AM, Siegel ER, Suva LJ, Ferrone S, Kieber-Emmons T, Monzavi-Karbassi B: Chondroitin sulfates play a major role in breast cancer metastasis: a role for CSPG4 and CHST11 gene expression in forming surface P-selectin ligands in aggressive breast cancer cells. Breast Cancer Res. 2011, 13: R58-10.1186/bcr2895.CrossRefPubMedPubMedCentral Cooney CA, Jousheghany F, Yao-Borengasser A, Phanavanh B, Gomes T, Kieber-Emmons AM, Siegel ER, Suva LJ, Ferrone S, Kieber-Emmons T, Monzavi-Karbassi B: Chondroitin sulfates play a major role in breast cancer metastasis: a role for CSPG4 and CHST11 gene expression in forming surface P-selectin ligands in aggressive breast cancer cells. Breast Cancer Res. 2011, 13: R58-10.1186/bcr2895.CrossRefPubMedPubMedCentral
33.
go back to reference Liapis H, Flath A, Kitazawa S: Integrin alpha V beta 3 expression by bone-residing breast cancer metastases. Diagn Mol Pathol. 1996, 5: 127-135. 10.1097/00019606-199606000-00008.CrossRefPubMed Liapis H, Flath A, Kitazawa S: Integrin alpha V beta 3 expression by bone-residing breast cancer metastases. Diagn Mol Pathol. 1996, 5: 127-135. 10.1097/00019606-199606000-00008.CrossRefPubMed
34.
go back to reference Belloc C, Lu H, Soria C, Fridman R, Legrand Y, Menashi S: The effect of platelets on invasiveness and protease production of human mammary tumor cells. Int J Cancer. 1995, 60: 413-417. 10.1002/ijc.2910600324.CrossRefPubMed Belloc C, Lu H, Soria C, Fridman R, Legrand Y, Menashi S: The effect of platelets on invasiveness and protease production of human mammary tumor cells. Int J Cancer. 1995, 60: 413-417. 10.1002/ijc.2910600324.CrossRefPubMed
35.
go back to reference Bambace NM, Levis JE, Holmes CE: The effect of P2Y-mediated platelet activation on the release of VEGF and endostatin from platelets. Platelets. 2010, 21: 85-93. 10.3109/09537100903470298.CrossRefPubMed Bambace NM, Levis JE, Holmes CE: The effect of P2Y-mediated platelet activation on the release of VEGF and endostatin from platelets. Platelets. 2010, 21: 85-93. 10.3109/09537100903470298.CrossRefPubMed
36.
go back to reference Peterson JE, Zurakowski D, Italiano JE, Michel LV, Fox L, Klement GL, Folkman J: Normal ranges of angiogenesis regulatory proteins in human platelets. Am J Hematol. 2010, 85: 487-493. 10.1002/ajh.21732.CrossRefPubMed Peterson JE, Zurakowski D, Italiano JE, Michel LV, Fox L, Klement GL, Folkman J: Normal ranges of angiogenesis regulatory proteins in human platelets. Am J Hematol. 2010, 85: 487-493. 10.1002/ajh.21732.CrossRefPubMed
37.
go back to reference Holmes CE, Huang JC, Pace TR, Howard AB, Muss HB: Tamoxifen and aromatase inhibitors differentially affect vascular endothelial growth factor and endostatin levels in women with breast cancer. Clin Cancer Res. 2008, 14: 3070-3076. 10.1158/1078-0432.CCR-07-4640.CrossRefPubMed Holmes CE, Huang JC, Pace TR, Howard AB, Muss HB: Tamoxifen and aromatase inhibitors differentially affect vascular endothelial growth factor and endostatin levels in women with breast cancer. Clin Cancer Res. 2008, 14: 3070-3076. 10.1158/1078-0432.CCR-07-4640.CrossRefPubMed
38.
go back to reference Italiano JE, 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: 1227-1233.CrossRefPubMedPubMedCentral Italiano JE, 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: 1227-1233.CrossRefPubMedPubMedCentral
39.
go back to reference Ho-Tin-Noe B, Carbo C, Demers M, Cifuni SM, Goerge T, Wagner DD: Innate immune cells induce hemorrhage in tumors during thrombocytopenia. Am J Pathol. 2009, 175: 1699-1708. 10.2353/ajpath.2009.090460.CrossRefPubMedPubMedCentral Ho-Tin-Noe B, Carbo C, Demers M, Cifuni SM, Goerge T, Wagner DD: Innate immune cells induce hemorrhage in tumors during thrombocytopenia. Am J Pathol. 2009, 175: 1699-1708. 10.2353/ajpath.2009.090460.CrossRefPubMedPubMedCentral
40.
go back to reference Demers M, Ho-Tin-Noe B, Schatzberg D, Yang JJ, Wagner DD: Increased efficacy of breast cancer chemotherapy in thrombocytopenic mice. Cancer Res. 2011, 71: 1540-1549. 10.1158/0008-5472.CAN-10-2038.CrossRefPubMedPubMedCentral Demers M, Ho-Tin-Noe B, Schatzberg D, Yang JJ, Wagner DD: Increased efficacy of breast cancer chemotherapy in thrombocytopenic mice. Cancer Res. 2011, 71: 1540-1549. 10.1158/0008-5472.CAN-10-2038.CrossRefPubMedPubMedCentral
41.
go back to reference Holmes MD, Chen WY, Li L, Hertzmark E, Spiegelman D, Hankinson SE: Aspirin intake and survival after breast cancer. J Clin Oncol. 2010, 28: 1467-1472. 10.1200/JCO.2009.22.7918.CrossRefPubMedPubMedCentral Holmes MD, Chen WY, Li L, Hertzmark E, Spiegelman D, Hankinson SE: Aspirin intake and survival after breast cancer. J Clin Oncol. 2010, 28: 1467-1472. 10.1200/JCO.2009.22.7918.CrossRefPubMedPubMedCentral
42.
go back to reference Takkouche B, Regueira-Mendez C, Etminan M: Breast cancer and use of nonsteroidal anti-inflammatory drugs: a meta-analysis. J Natl Cancer Inst. 2008, 100: 1439-1447. 10.1093/jnci/djn324.CrossRefPubMed Takkouche B, Regueira-Mendez C, Etminan M: Breast cancer and use of nonsteroidal anti-inflammatory drugs: a meta-analysis. J Natl Cancer Inst. 2008, 100: 1439-1447. 10.1093/jnci/djn324.CrossRefPubMed
43.
44.
go back to reference Rothwell PM, Wilson M, Price JF, Belch JF, Meade TW, Mehta Z: Effect of daily aspirin on risk of cancer metastasis: a study of incident cancers during randomised controlled trials. Lancet. 2012, 379: 1591-1601. 10.1016/S0140-6736(12)60209-8.CrossRefPubMed Rothwell PM, Wilson M, Price JF, Belch JF, Meade TW, Mehta Z: Effect of daily aspirin on risk of cancer metastasis: a study of incident cancers during randomised controlled trials. Lancet. 2012, 379: 1591-1601. 10.1016/S0140-6736(12)60209-8.CrossRefPubMed
45.
go back to reference van den Berg YW, Osanto S, Reitsma PH, Versteeg HH: The relationship between tissue factor and cancer progression: insights from bench and bedside. Blood. 2012, 119: 924-932. 10.1182/blood-2011-06-317685.CrossRefPubMed van den Berg YW, Osanto S, Reitsma PH, Versteeg HH: The relationship between tissue factor and cancer progression: insights from bench and bedside. Blood. 2012, 119: 924-932. 10.1182/blood-2011-06-317685.CrossRefPubMed
46.
47.
go back to reference Ueno T, Toi M, Koike M, Nakamura S, Tominaga T: Tissue factor expression in breast cancer tissues: its correlation with prognosis and plasma concentration. Br J Cancer. 2000, 83: 164-170.CrossRefPubMedPubMedCentral Ueno T, Toi M, Koike M, Nakamura S, Tominaga T: Tissue factor expression in breast cancer tissues: its correlation with prognosis and plasma concentration. Br J Cancer. 2000, 83: 164-170.CrossRefPubMedPubMedCentral
48.
go back to reference Hu C, Huang L, Gest C, Xi X, Janin A, Soria C, Li H, Lu H: Opposite regulation by PI3K/Akt and MAPK/ERK pathways of tissue factor expression, cell-associated procoagulant activity and invasiveness in MDA-MB-231 cells. J Hematol Oncol. 2012, 5: 16-10.1186/1756-8722-5-16.CrossRefPubMedPubMedCentral Hu C, Huang L, Gest C, Xi X, Janin A, Soria C, Li H, Lu H: Opposite regulation by PI3K/Akt and MAPK/ERK pathways of tissue factor expression, cell-associated procoagulant activity and invasiveness in MDA-MB-231 cells. J Hematol Oncol. 2012, 5: 16-10.1186/1756-8722-5-16.CrossRefPubMedPubMedCentral
49.
go back to reference Ryden L, Grabau D, Schaffner F, Jonsson PE, Ruf W, Belting M: Evidence for tissue factor phosphorylation and its correlation with protease-activated receptor expression and the prognosis of primary breast cancer. Int J Cancer. 2010, 126: 2330-2340.PubMedPubMedCentral Ryden L, Grabau D, Schaffner F, Jonsson PE, Ruf W, Belting M: Evidence for tissue factor phosphorylation and its correlation with protease-activated receptor expression and the prognosis of primary breast cancer. Int J Cancer. 2010, 126: 2330-2340.PubMedPubMedCentral
50.
go back to reference Vrana JA, Stang MT, Grande JP, Getz MJ: Expression of tissue factor in tumor stroma correlates with progression to invasive human breast cancer: paracrine regulation by carcinoma cell-derived members of the transforming growth factor beta family. Cancer Res. 1996, 56: 5063-5070.PubMed Vrana JA, Stang MT, Grande JP, Getz MJ: Expression of tissue factor in tumor stroma correlates with progression to invasive human breast cancer: paracrine regulation by carcinoma cell-derived members of the transforming growth factor beta family. Cancer Res. 1996, 56: 5063-5070.PubMed
51.
go back to reference Albrektsen T, Sorensen BB, Hjorto GM, Fleckner J, Rao LV, Petersen LC: Transcriptional program induced by factor VIIa-tissue factor, PAR1 and PAR2 in MDA-MB-231 cells. J Thromb Haemost. 2007, 5: 1588-1597. 10.1111/j.1538-7836.2007.02603.x.CrossRefPubMedPubMedCentral Albrektsen T, Sorensen BB, Hjorto GM, Fleckner J, Rao LV, Petersen LC: Transcriptional program induced by factor VIIa-tissue factor, PAR1 and PAR2 in MDA-MB-231 cells. J Thromb Haemost. 2007, 5: 1588-1597. 10.1111/j.1538-7836.2007.02603.x.CrossRefPubMedPubMedCentral
52.
go back to reference Zwicker JI, Liebman HA, Neuberg D, Lacroix R, Bauer KA, Furie BC, Furie B: Tumor-derived tissue factor-bearing microparticles are associated with venous thromboembolic events in malignancy. Clin Cancer Res. 2009, 15: 6830-6840. 10.1158/1078-0432.CCR-09-0371.CrossRefPubMedPubMedCentral Zwicker JI, Liebman HA, Neuberg D, Lacroix R, Bauer KA, Furie BC, Furie B: Tumor-derived tissue factor-bearing microparticles are associated with venous thromboembolic events in malignancy. Clin Cancer Res. 2009, 15: 6830-6840. 10.1158/1078-0432.CCR-09-0371.CrossRefPubMedPubMedCentral
53.
go back to reference Tesselaar ME, Romijn FP, Van Der Linden IK, Prins FA, Bertina RM, Osanto S: Microparticle-associated tissue factor activity: a link between cancer and thrombosis?. J Thromb Haemost. 2007, 5: 520-527. 10.1111/j.1538-7836.2007.02369.x.CrossRefPubMed Tesselaar ME, Romijn FP, Van Der Linden IK, Prins FA, Bertina RM, Osanto S: Microparticle-associated tissue factor activity: a link between cancer and thrombosis?. J Thromb Haemost. 2007, 5: 520-527. 10.1111/j.1538-7836.2007.02369.x.CrossRefPubMed
54.
go back to reference Versteeg HH, Schaffner F, Kerver M, Petersen HH, Ahamed J, Felding-Habermann B, Takada Y, Mueller BM, Ruf W: Inhibition of tissue factor signaling suppresses tumor growth. Blood. 2008, 111: 190-199. 10.1182/blood-2007-07-101048.CrossRefPubMedPubMedCentral Versteeg HH, Schaffner F, Kerver M, Petersen HH, Ahamed J, Felding-Habermann B, Takada Y, Mueller BM, Ruf W: Inhibition of tissue factor signaling suppresses tumor growth. Blood. 2008, 111: 190-199. 10.1182/blood-2007-07-101048.CrossRefPubMedPubMedCentral
55.
56.
go back to reference Marchetti M, Russo L, Balducci D, Falanga A: All trans-retinoic acid modulates the procoagulant activity of human breast cancer cells. Thromb Res. 2011, 128: 368-374. 10.1016/j.thromres.2011.03.006.CrossRefPubMed Marchetti M, Russo L, Balducci D, Falanga A: All trans-retinoic acid modulates the procoagulant activity of human breast cancer cells. Thromb Res. 2011, 128: 368-374. 10.1016/j.thromres.2011.03.006.CrossRefPubMed
57.
go back to reference Falanga A, Toma S, Marchetti M, Palumbo R, Raffo P, Consonni R, Marziali S, Dastoli G, Barbui T: Effect of all-trans-retinoic acid on the hypercoagulable state of patients with breast cancer. Am J Hematol. 2002, 70: 9-15. 10.1002/ajh.10073.CrossRefPubMed Falanga A, Toma S, Marchetti M, Palumbo R, Raffo P, Consonni R, Marziali S, Dastoli G, Barbui T: Effect of all-trans-retinoic acid on the hypercoagulable state of patients with breast cancer. Am J Hematol. 2002, 70: 9-15. 10.1002/ajh.10073.CrossRefPubMed
58.
go back to reference Shoji M, Sun A, Kisiel W, Lu YJ, Shim H, McCarey BE, Nichols C, Parker ET, Pohl J, Mosley CA, Alizadeh AR, Liotta DC, Snyder JP: Targeting tissue factor-expressing tumor angiogenesis and tumors with EF24 conjugated to factor VIIa. J Drug Target. 2008, 16: 185-197. 10.1080/10611860801890093.CrossRefPubMed Shoji M, Sun A, Kisiel W, Lu YJ, Shim H, McCarey BE, Nichols C, Parker ET, Pohl J, Mosley CA, Alizadeh AR, Liotta DC, Snyder JP: Targeting tissue factor-expressing tumor angiogenesis and tumors with EF24 conjugated to factor VIIa. J Drug Target. 2008, 16: 185-197. 10.1080/10611860801890093.CrossRefPubMed
59.
go back to reference Yu JL, Xing R, Milsom C, Rak J: Modulation of the oncogene-dependent tissue factor expression by kinase suppressor of ras 1. Thromb Res. 2010, 126: e6-10. 10.1016/j.thromres.2010.04.014.CrossRefPubMed Yu JL, Xing R, Milsom C, Rak J: Modulation of the oncogene-dependent tissue factor expression by kinase suppressor of ras 1. Thromb Res. 2010, 126: e6-10. 10.1016/j.thromres.2010.04.014.CrossRefPubMed
60.
go back to reference Zhang X, Yu H, Lou JR, Zheng J, Zhu H, Popescu NI, Lupu F, Lind SE, Ding WQ: MicroRNA-19 (miR-19) regulates tissue factor expression in breast cancer cells. J Biol Chem. 2011, 286: 1429-1435. 10.1074/jbc.M110.146530.CrossRefPubMed Zhang X, Yu H, Lou JR, Zheng J, Zhu H, Popescu NI, Lupu F, Lind SE, Ding WQ: MicroRNA-19 (miR-19) regulates tissue factor expression in breast cancer cells. J Biol Chem. 2011, 286: 1429-1435. 10.1074/jbc.M110.146530.CrossRefPubMed
61.
go back to reference Koizume S, Jin MS, Miyagi E, Hirahara F, Nakamura Y, Piao JH, Asai A, Yoshida A, Tsuchiya E, Ruf W, Miyagi Y: Activation of cancer cell migration and invasion by ectopic synthesis of coagulation factor VII. Cancer Res. 2006, 66: 9453-9460. 10.1158/0008-5472.CAN-06-1803.CrossRefPubMed Koizume S, Jin MS, Miyagi E, Hirahara F, Nakamura Y, Piao JH, Asai A, Yoshida A, Tsuchiya E, Ruf W, Miyagi Y: Activation of cancer cell migration and invasion by ectopic synthesis of coagulation factor VII. Cancer Res. 2006, 66: 9453-9460. 10.1158/0008-5472.CAN-06-1803.CrossRefPubMed
62.
go back to reference Contrino J, Hair G, Kreutzer DL, Rickles FR: In situ detection of tissue factor in vascular endothelial cells: correlation with the malignant phenotype of human breast disease. Nat Med. 1996, 2: 209-215. 10.1038/nm0296-209.CrossRefPubMed Contrino J, Hair G, Kreutzer DL, Rickles FR: In situ detection of tissue factor in vascular endothelial cells: correlation with the malignant phenotype of human breast disease. Nat Med. 1996, 2: 209-215. 10.1038/nm0296-209.CrossRefPubMed
63.
go back to reference Garnier D, Magnus N, D'Asti E, Hashemi M, Meehan B, Milsom C, Rak J: Genetic pathways linking hemostasis and cancer. Thromb Res. 2012, 129 (Suppl 1): S22-29.CrossRefPubMed Garnier D, Magnus N, D'Asti E, Hashemi M, Meehan B, Milsom C, Rak J: Genetic pathways linking hemostasis and cancer. Thromb Res. 2012, 129 (Suppl 1): S22-29.CrossRefPubMed
64.
go back to reference Jiang X, Zhu S, Panetti TS, Bromberg ME: Formation of tissue factor-factor VIIa-factor Xa complex induces activation of the mTOR pathway which regulates migration of human breast cancer cells. Thromb Haemost. 2008, 100: 127-133.PubMed Jiang X, Zhu S, Panetti TS, Bromberg ME: Formation of tissue factor-factor VIIa-factor Xa complex induces activation of the mTOR pathway which regulates migration of human breast cancer cells. Thromb Haemost. 2008, 100: 127-133.PubMed
65.
go back to reference Hjortoe GM, Petersen LC, Albrektsen T, Sorensen BB, Norby PL, Mandal SK, Pendurthi UR, Rao LV: Tissue factor-factor VIIa-specific up-regulation of IL-8 expression in MDA-MB-231 cells is mediated by PAR-2 and results in increased cell migration. Blood. 2004, 103: 3029-3037. 10.1182/blood-2003-10-3417.CrossRefPubMedPubMedCentral Hjortoe GM, Petersen LC, Albrektsen T, Sorensen BB, Norby PL, Mandal SK, Pendurthi UR, Rao LV: Tissue factor-factor VIIa-specific up-regulation of IL-8 expression in MDA-MB-231 cells is mediated by PAR-2 and results in increased cell migration. Blood. 2004, 103: 3029-3037. 10.1182/blood-2003-10-3417.CrossRefPubMedPubMedCentral
66.
go back to reference Coughlin SR: Thrombin signalling and protease-activated receptors. Nature. 2000, 407: 258-264. 10.1038/35025229.CrossRefPubMed Coughlin SR: Thrombin signalling and protease-activated receptors. Nature. 2000, 407: 258-264. 10.1038/35025229.CrossRefPubMed
67.
go back to reference Even-Ram S, Uziely B, Cohen P, Grisaru-Granovsky S, Maoz M, Ginzburg Y, Reich R, Vlodavsky I, Bar-Shavit R: Thrombin receptor overexpression in malignant and physiological invasion processes. Nat Med. 1998, 4: 909-914. 10.1038/nm0898-909.CrossRefPubMed Even-Ram S, Uziely B, Cohen P, Grisaru-Granovsky S, Maoz M, Ginzburg Y, Reich R, Vlodavsky I, Bar-Shavit R: Thrombin receptor overexpression in malignant and physiological invasion processes. Nat Med. 1998, 4: 909-914. 10.1038/nm0898-909.CrossRefPubMed
68.
go back to reference Hu L, Lee M, Campbell W, Perez-Soler R, Karpatkin S: Role of endogenous thrombin in tumor implantation, seeding, and spontaneous metastasis. Blood. 2004, 104: 2746-2751. 10.1182/blood-2004-03-1047.CrossRefPubMed Hu L, Lee M, Campbell W, Perez-Soler R, Karpatkin S: Role of endogenous thrombin in tumor implantation, seeding, and spontaneous metastasis. Blood. 2004, 104: 2746-2751. 10.1182/blood-2004-03-1047.CrossRefPubMed
69.
go back to reference DeFeo K, Hayes C, Chernick M, Ryn JV, Gilmour SK: Use of dabigatran etexilate to reduce breast cancer progression. Cancer Biol Ther. 2010, 10: 1001-1008. 10.4161/cbt.10.10.13236.CrossRefPubMed DeFeo K, Hayes C, Chernick M, Ryn JV, Gilmour SK: Use of dabigatran etexilate to reduce breast cancer progression. Cancer Biol Ther. 2010, 10: 1001-1008. 10.4161/cbt.10.10.13236.CrossRefPubMed
70.
go back to reference Caunt M, Hu L, Tang T, Brooks PC, Ibrahim S, Karpatkin S: Growth-regulated oncogene is pivotal in thrombin-induced angiogenesis. Cancer Res. 2006, 66: 4125-4132. 10.1158/0008-5472.CAN-05-2570.CrossRefPubMed Caunt M, Hu L, Tang T, Brooks PC, Ibrahim S, Karpatkin S: Growth-regulated oncogene is pivotal in thrombin-induced angiogenesis. Cancer Res. 2006, 66: 4125-4132. 10.1158/0008-5472.CAN-05-2570.CrossRefPubMed
71.
go back to reference Schaffner F, Versteeg HH, Schillert A, Yokota N, Petersen LC, Mueller BM, Ruf W: Cooperation of tissue factor cytoplasmic domain and PAR2 signaling in breast cancer development. Blood. 2010, 116: 6106-6113. 10.1182/blood-2010-06-289314.CrossRefPubMedPubMedCentral Schaffner F, Versteeg HH, Schillert A, Yokota N, Petersen LC, Mueller BM, Ruf W: Cooperation of tissue factor cytoplasmic domain and PAR2 signaling in breast cancer development. Blood. 2010, 116: 6106-6113. 10.1182/blood-2010-06-289314.CrossRefPubMedPubMedCentral
72.
go back to reference 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. 10.1016/j.ccr.2006.10.002.CrossRefPubMed 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. 10.1016/j.ccr.2006.10.002.CrossRefPubMed
73.
go back to reference Rak J, Milsom C, May L, Klement P, Yu J: Tissue factor in cancer and angiogenesis: the molecular link between genetic tumor progression, tumor neovascularization, and cancer coagulopathy. Semin Thromb Hemost. 2006, 32: 54-70. 10.1055/s-2006-933341.CrossRefPubMed Rak J, Milsom C, May L, Klement P, Yu J: Tissue factor in cancer and angiogenesis: the molecular link between genetic tumor progression, tumor neovascularization, and cancer coagulopathy. Semin Thromb Hemost. 2006, 32: 54-70. 10.1055/s-2006-933341.CrossRefPubMed
74.
go back to reference Han B, Nakamura M, Mori I, Nakamura Y, Kakudo K: Urokinase-type plasminogen activator system and breast cancer (Review). Oncol Rep. 2005, 14: 105-112.PubMed Han B, Nakamura M, Mori I, Nakamura Y, Kakudo K: Urokinase-type plasminogen activator system and breast cancer (Review). Oncol Rep. 2005, 14: 105-112.PubMed
75.
go back to reference Look MP, van Putten WL, Duffy MJ, Harbeck N, Christensen IJ, Thomssen C, Kates R, Spyratos F, Fernö M, Eppenberger-Castori S, Sweep CG, Ulm K, Peyrat JP, Martin PM, Magdelenat H, Brünner N, Duggan C, Lisboa BW, Bendahl PO, Quillien V, Daver A, Ricolleau G, Meijer-van Gelder ME, Manders P, Fiets WE, Blankenstein MA, Broët P, Romain S, Daxenbichler G, Windbichler G, et al: Pooled analysis of prognostic impact of urokinase-type plasminogen activator and its inhibitor PAI-1 in 8377 breast cancer patients. J Natl Cancer Inst. 2002, 94: 116-128. 10.1093/jnci/94.2.116.CrossRefPubMed Look MP, van Putten WL, Duffy MJ, Harbeck N, Christensen IJ, Thomssen C, Kates R, Spyratos F, Fernö M, Eppenberger-Castori S, Sweep CG, Ulm K, Peyrat JP, Martin PM, Magdelenat H, Brünner N, Duggan C, Lisboa BW, Bendahl PO, Quillien V, Daver A, Ricolleau G, Meijer-van Gelder ME, Manders P, Fiets WE, Blankenstein MA, Broët P, Romain S, Daxenbichler G, Windbichler G, et al: Pooled analysis of prognostic impact of urokinase-type plasminogen activator and its inhibitor PAI-1 in 8377 breast cancer patients. J Natl Cancer Inst. 2002, 94: 116-128. 10.1093/jnci/94.2.116.CrossRefPubMed
76.
go back to reference Wolff C, Malinowsky K, Berg D, Schragner K, Schuster T, Walch A, Bronger H, Hofier H, Becker KF: Signalling networks associated with urokinase-type plasminogen activator (uPA) and its inhibitor PAI-1 in breast cancer tissues: new insights from protein microarray analysis. J Pathol. 2011, 223: 54-63. 10.1002/path.2791.CrossRefPubMed Wolff C, Malinowsky K, Berg D, Schragner K, Schuster T, Walch A, Bronger H, Hofier H, Becker KF: Signalling networks associated with urokinase-type plasminogen activator (uPA) and its inhibitor PAI-1 in breast cancer tissues: new insights from protein microarray analysis. J Pathol. 2011, 223: 54-63. 10.1002/path.2791.CrossRefPubMed
77.
go back to reference Malinowsky K, Wolff C, Berg D, Schuster T, Walch A, Bronger H, Mannsperger H, Schmidt C, Korf U, Höfler H, Becker KF: uPA and PAI-1-Related Signaling Pathways Differ between Primary Breast Cancers and Lymph Node Metastases. Transl Oncol. 2012, 5: 98-104.CrossRefPubMedPubMedCentral Malinowsky K, Wolff C, Berg D, Schuster T, Walch A, Bronger H, Mannsperger H, Schmidt C, Korf U, Höfler H, Becker KF: uPA and PAI-1-Related Signaling Pathways Differ between Primary Breast Cancers and Lymph Node Metastases. Transl Oncol. 2012, 5: 98-104.CrossRefPubMedPubMedCentral
78.
go back to reference Hurst NJ, Najy AJ, Ustach CV, Movilla L, Kim HR: Platelet-derived growth factor-C (PDGF-C) activation by serine proteases: implications for breast cancer progression. Biochem J. 2012, 441: 909-918. 10.1042/BJ20111020.CrossRefPubMedPubMedCentral Hurst NJ, Najy AJ, Ustach CV, Movilla L, Kim HR: Platelet-derived growth factor-C (PDGF-C) activation by serine proteases: implications for breast cancer progression. Biochem J. 2012, 441: 909-918. 10.1042/BJ20111020.CrossRefPubMedPubMedCentral
79.
go back to reference Bajou K, Lewalle JM, Martinez CR, Soria C, Lu H, Noel A, Foidart JM: Human breast adenocarcinoma cell lines promote angiogenesis by providing cells with uPA-PAI-1 and by enhancing their expression. Int J Cancer. 2002, 100: 501-506. 10.1002/ijc.10487.CrossRefPubMed Bajou K, Lewalle JM, Martinez CR, Soria C, Lu H, Noel A, Foidart JM: Human breast adenocarcinoma cell lines promote angiogenesis by providing cells with uPA-PAI-1 and by enhancing their expression. Int J Cancer. 2002, 100: 501-506. 10.1002/ijc.10487.CrossRefPubMed
80.
go back to reference Kakkar AK, Levine MN, Kadziola Z, Lemoine NR, Low V, Patel HK, Rustin G, Thomas M, Quigley M, Williamson RC: Low molecular weight heparin, therapy with dalteparin, and survival in advanced cancer: the fragmin advanced malignancy outcome study (FAMOUS). J Clin Oncol. 2004, 22: 1944-1948. 10.1200/JCO.2004.10.002.CrossRefPubMed Kakkar AK, Levine MN, Kadziola Z, Lemoine NR, Low V, Patel HK, Rustin G, Thomas M, Quigley M, Williamson RC: Low molecular weight heparin, therapy with dalteparin, and survival in advanced cancer: the fragmin advanced malignancy outcome study (FAMOUS). J Clin Oncol. 2004, 22: 1944-1948. 10.1200/JCO.2004.10.002.CrossRefPubMed
81.
go back to reference Sideras K, Schaefer PL, Okuno SH, Sloan JA, Kutteh L, Fitch TR, Dakhil SR, Levitt R, Alberts SR, Morton RF, Rowland KM, Novotny PJ, Loprinzi CL: Low-molecular-weight heparin in patients with advanced cancer: a phase 3 clinical trial. Mayo Clin Proc. 2006, 81: 758-767. 10.4065/81.6.758.CrossRefPubMed Sideras K, Schaefer PL, Okuno SH, Sloan JA, Kutteh L, Fitch TR, Dakhil SR, Levitt R, Alberts SR, Morton RF, Rowland KM, Novotny PJ, Loprinzi CL: Low-molecular-weight heparin in patients with advanced cancer: a phase 3 clinical trial. Mayo Clin Proc. 2006, 81: 758-767. 10.4065/81.6.758.CrossRefPubMed
82.
go back to reference Klerk CP, Smorenburg SM, Otten HM, Lensing AW, Prins MH, Piovella F, Prandoni P, Bos MM, Richel DJ, van Tienhoven G, Büller HR: The effect of low molecular weight heparin on survival in patients with advanced malignancy. J Clin Oncol. 2005, 23: 2130-2135. 10.1200/JCO.2005.03.134.CrossRefPubMed Klerk CP, Smorenburg SM, Otten HM, Lensing AW, Prins MH, Piovella F, Prandoni P, Bos MM, Richel DJ, van Tienhoven G, Büller HR: The effect of low molecular weight heparin on survival in patients with advanced malignancy. J Clin Oncol. 2005, 23: 2130-2135. 10.1200/JCO.2005.03.134.CrossRefPubMed
83.
go back to reference Agnelli G, Gussoni G, Bianchini C, Verso M, Mandalà M, Cavanna L, Barni S, Labianca R, Buzzi F, Scambia G, Passalacqua R, Ricci S, Gasparini G, Lorusso V, Bonizzoni E, Tonato M, PROTECHT Investigators: Nadroparin for the prevention of thromboembolic events in ambulatory patients with metastatic or locally advanced solid cancer receiving chemotherapy: a randomised, placebo-controlled, double-blind study. Lancet Oncol. 2009, 10: 943-949. 10.1016/S1470-2045(09)70232-3.CrossRefPubMed Agnelli G, Gussoni G, Bianchini C, Verso M, Mandalà M, Cavanna L, Barni S, Labianca R, Buzzi F, Scambia G, Passalacqua R, Ricci S, Gasparini G, Lorusso V, Bonizzoni E, Tonato M, PROTECHT Investigators: Nadroparin for the prevention of thromboembolic events in ambulatory patients with metastatic or locally advanced solid cancer receiving chemotherapy: a randomised, placebo-controlled, double-blind study. Lancet Oncol. 2009, 10: 943-949. 10.1016/S1470-2045(09)70232-3.CrossRefPubMed
84.
go back to reference Levine M, Hirsh J, Gent M, Arnold A, Warr D, Falanga A, Samosh M, Bramwell V, Pritchard KI, Stewart D, et al: Double-blind randomised trial of a very-low-dose warfarin for prevention of thromboembolism in stage IV breast cancer. Lancet. 1994, 343: 886-889. 10.1016/S0140-6736(94)90008-6.CrossRefPubMed Levine M, Hirsh J, Gent M, Arnold A, Warr D, Falanga A, Samosh M, Bramwell V, Pritchard KI, Stewart D, et al: Double-blind randomised trial of a very-low-dose warfarin for prevention of thromboembolism in stage IV breast cancer. Lancet. 1994, 343: 886-889. 10.1016/S0140-6736(94)90008-6.CrossRefPubMed
85.
go back to reference Golubkov VS, Strongin AY: Proteolysis-driven oncogenesis. Cell Cycle. 2007, 6: 147-150. 10.4161/cc.6.2.3706.CrossRefPubMed Golubkov VS, Strongin AY: Proteolysis-driven oncogenesis. Cell Cycle. 2007, 6: 147-150. 10.4161/cc.6.2.3706.CrossRefPubMed
86.
go back to reference Jiang X, Guo YL, Bromberg ME: Formation of tissue factor-factor VIIa-factor Xa complex prevents apoptosis in human breast cancer cells. Thromb Haemost. 2006, 96: 196-201.PubMed Jiang X, Guo YL, Bromberg ME: Formation of tissue factor-factor VIIa-factor Xa complex prevents apoptosis in human breast cancer cells. Thromb Haemost. 2006, 96: 196-201.PubMed
87.
go back to reference Powles TJ, Dady PJ, Williams J, Easty GC, Coombes RC: Use of inhibitors of prostaglandin synthesis in patients with breast cancer. Adv Prostaglandin Thromboxane Res. 1980, 6: 511-516.PubMed Powles TJ, Dady PJ, Williams J, Easty GC, Coombes RC: Use of inhibitors of prostaglandin synthesis in patients with breast cancer. Adv Prostaglandin Thromboxane Res. 1980, 6: 511-516.PubMed
Metadata
Title
Platelets, coagulation and fibrinolysis in breast cancer progression
Authors
Inder Lal
Kim Dittus
Chris E Holmes
Publication date
01-08-2013
Publisher
BioMed Central
Published in
Breast Cancer Research / Issue 4/2013
Electronic ISSN: 1465-542X
DOI
https://doi.org/10.1186/bcr3425

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