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Published in: Journal of Cancer Research and Clinical Oncology 1/2014

01-01-2014 | Original Paper

Elevated circulating levels of tissue factor-positive microvesicles are associated with distant metastasis in lung cancer

Authors: Jo-Chi Tseng, Liang-Che Chang, Boy-Yiing Jiang, Yu-Chih Liu, Hung-Jie Chen, Chih-Teng Yu, Chung-Ching Hua

Published in: Journal of Cancer Research and Clinical Oncology | Issue 1/2014

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Abstract

Purpose

Microvesicles (MV) in the blood stream are associated with distant metastasis in cancer. Platelet or endothelial cell-related MV actively participate in thrombogenesis, which is an important step in cancer metastasis. This study investigated the correlations between MV levels of platelet-poor plasma and distant metastasis in lung cancer.

Methods

Platelet-poor plasma from 44 treatment-naive lung cancer (23 with distant metastasis) and 19 normal subjects was used to determine the levels of glycoprotein Iβ (CD42) + platelet MV (PMV), P-selectin (CD62P) + PMV, VE-cadherin (CD144) + endothelial MV (EMV), tissue factor (CD142) + MV, thrombin-antithrombin complex and vascular endothelial growth factor (VEGF).

Results

The level of CD142 + MV was significant (odds ratio 5.86, 95 % confidence interval 1.31–38.3) in predicting distant metastasis in lung cancer, and a cutoff value of 2.668 (after logarithm transformation) in the ROC curve had a specificity of 90 % and a sensitivity of 59 %. The presence of distant metastasis showed a significant correlation between CD144 + EMV and VEGF, but not between CD144 + EMV and CD42 + PMV or CD62P + PMV in lung cancer subjects.

Conclusions

The finding of CD142 + MV in platelet-poor plasma may be useful for suggesting distant metastasis in lung cancer. In addition to thrombogenesis, interaction between VE-cadherin and VEGF may be needed for successful metastasis in lung cancer.
Literature
go back to reference Al-Nedawi K, Meehan B, Kerbel RS, Allison AC, Rak J (2009) Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc Natl Acad Sci 106(10):3794–3799. doi:10.1073/pnas.0804543106 PubMedCrossRef Al-Nedawi K, Meehan B, Kerbel RS, Allison AC, Rak J (2009) Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc Natl Acad Sci 106(10):3794–3799. doi:10.​1073/​pnas.​0804543106 PubMedCrossRef
go back to reference Amabile N, Guérin AP, Leroyer A, Mallat Z, Nguyen C, Boddaert J, London GM, Tedgui A, Boulanger CM (2005) Circulating endothelial microparticles are associated with vascular dysfunction in patients with end-stage renal failure. J Am Soc Nephrol 16(11):3381–3388. doi:10.1681/asn.2005050535 PubMedCrossRef Amabile N, Guérin AP, Leroyer A, Mallat Z, Nguyen C, Boddaert J, London GM, Tedgui A, Boulanger CM (2005) Circulating endothelial microparticles are associated with vascular dysfunction in patients with end-stage renal failure. J Am Soc Nephrol 16(11):3381–3388. doi:10.​1681/​asn.​2005050535 PubMedCrossRef
go back to reference Amirkhosravi A, Meyer T, Amaya M, Davila M, Mousa SA, Robson T, Francis JL (2007) The role of tissue factor pathway inhibitor in tumor growth and metastasis. Semin Thromb Hemost 33(7):643–652. doi:10.1055/s-2007-991531 PubMedCrossRef Amirkhosravi A, Meyer T, Amaya M, Davila M, Mousa SA, Robson T, Francis JL (2007) The role of tissue factor pathway inhibitor in tumor growth and metastasis. Semin Thromb Hemost 33(7):643–652. doi:10.​1055/​s-2007-991531 PubMedCrossRef
go back to reference Asakura H, Hifumi S, Jokaji H, Saito M, Kumabashiri I, Uotani C, Morishita E, Yamazaki M, Shibata K, Mizuhashi K (1992) Prothrombin fragment F1 + 2 and thrombin-antithrombin III complex are useful markers of the hypercoagulable state in atrial fibrillation. Blood Coagul Fibrinolysis 3(4):469–473PubMed Asakura H, Hifumi S, Jokaji H, Saito M, Kumabashiri I, Uotani C, Morishita E, Yamazaki M, Shibata K, Mizuhashi K (1992) Prothrombin fragment F1 + 2 and thrombin-antithrombin III complex are useful markers of the hypercoagulable state in atrial fibrillation. Blood Coagul Fibrinolysis 3(4):469–473PubMed
go back to reference Boda-Heggemann J, Regnier-Vigouroux A, Franke WW (2009) Beyond vessels: occurrence and regional clustering of vascular endothelial (VE-) cadherin-containing junctions in non-endothelial cells. Cell Tissue Res 335(1):49–65. doi:10.1007/s00441-008-0718-1 PubMedCrossRef Boda-Heggemann J, Regnier-Vigouroux A, Franke WW (2009) Beyond vessels: occurrence and regional clustering of vascular endothelial (VE-) cadherin-containing junctions in non-endothelial cells. Cell Tissue Res 335(1):49–65. doi:10.​1007/​s00441-008-0718-1 PubMedCrossRef
go back to reference Chironi GN, Boulanger CM, Simon A, Dignat-George F, Freyssinet J-M, Tedgui A (2009) Endothelial microparticles in diseases. Cell Tissue Res 335(1):143–151PubMedCrossRef Chironi GN, Boulanger CM, Simon A, Dignat-George F, Freyssinet J-M, Tedgui A (2009) Endothelial microparticles in diseases. Cell Tissue Res 335(1):143–151PubMedCrossRef
go back to reference Fidler IJ (2003) The pathogenesis of cancer metastasis: the ‘seed and soil’ hypothesis revisited. Nat Rev Cancer 3(6):453–458PubMedCrossRef Fidler IJ (2003) The pathogenesis of cancer metastasis: the ‘seed and soil’ hypothesis revisited. Nat Rev Cancer 3(6):453–458PubMedCrossRef
go back to reference Gay LJ, Felding-Habermann B (2011) Contribution of platelets to tumour metastasis. Nat Rev Cancer 11(2):123–134PubMedCrossRef Gay LJ, Felding-Habermann B (2011) Contribution of platelets to tumour metastasis. Nat Rev Cancer 11(2):123–134PubMedCrossRef
go back to reference Grange C, Tapparo M, Collino F, Vitillo L, Damasco C, Deregibus MC, Tetta C, Bussolati B, Camussi G (2011) Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res 71(15):5346–5356. doi:10.1158/0008-5472.can-11-0241 PubMedCrossRef Grange C, Tapparo M, Collino F, Vitillo L, Damasco C, Deregibus MC, Tetta C, Bussolati B, Camussi G (2011) Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res 71(15):5346–5356. doi:10.​1158/​0008-5472.​can-11-0241 PubMedCrossRef
go back to reference Hron G, Kollars M, Weber H, Sagaster V, Quehenberger P, Eichinger S, Kyrle PA, Weltermann A (2007) Tissue factor-positive microparticles: cellular origin and association with coagulation activation in patients with colorectal cancer. Thromb Haemos 97(1):119–123. doi:10.1160/TH06-03-0141 Hron G, Kollars M, Weber H, Sagaster V, Quehenberger P, Eichinger S, Kyrle PA, Weltermann A (2007) Tissue factor-positive microparticles: cellular origin and association with coagulation activation in patients with colorectal cancer. Thromb Haemos 97(1):119–123. doi:10.​1160/​TH06-03-0141
go back to reference Janowska-Wieczorek A, Wysoczynski M, Kijowski J, Marquez-Curtis L, Machalinski B, Ratajczak J, Ratajczak MZ (2005) Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer. Int J Cancer 113(5):752–760. doi:10.1002/ijc.20657 PubMedCrossRef Janowska-Wieczorek A, Wysoczynski M, Kijowski J, Marquez-Curtis L, Machalinski B, Ratajczak J, Ratajczak MZ (2005) Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer. Int J Cancer 113(5):752–760. doi:10.​1002/​ijc.​20657 PubMedCrossRef
go back to reference Kim HK, Song KS, Park YS, Kang YH, Lee YJ, Lee KR, Kim HK, Ryu KW, Bae JM, Kim S (2003) Elevated levels of circulating platelet microparticles, VEGF, IL-6 and RANTES in patients with gastric cancer: possible role of a metastasis predictor. Eur J Cancer 39(2):184–191. doi:10.1016/S0959-8049(02)00596-8 PubMedCrossRef Kim HK, Song KS, Park YS, Kang YH, Lee YJ, Lee KR, Kim HK, Ryu KW, Bae JM, Kim S (2003) Elevated levels of circulating platelet microparticles, VEGF, IL-6 and RANTES in patients with gastric cancer: possible role of a metastasis predictor. Eur J Cancer 39(2):184–191. doi:10.​1016/​S0959-8049(02)00596-8 PubMedCrossRef
go back to reference Martin T, Mason M, Jiang W (2011) Tight junctions in cancer metastasis. Front Biosci 16:898CrossRef Martin T, Mason M, Jiang W (2011) Tight junctions in cancer metastasis. Front Biosci 16:898CrossRef
go back to reference Möhle R, Green D, Moore MAS, Nachman RL, Rafii S (1997) Constitutive production and thrombin-induced release of vascular endothelial growth factor by human megakaryocytes and platelets. Proc Natl Acad Sci 94(2):663–668PubMedCrossRef Möhle R, Green D, Moore MAS, Nachman RL, Rafii S (1997) Constitutive production and thrombin-induced release of vascular endothelial growth factor by human megakaryocytes and platelets. Proc Natl Acad Sci 94(2):663–668PubMedCrossRef
go back to reference Monroe D, Hoffman M, Roberts H (2010) Molecular biology and biochemistry of the coagulation factors and pathways of hemostasis. In: Prchal J, Kaushansky K, Lichtman M, Kipps T, Seligsohn U (eds) Williams hematology, 8th edn. McGraw-Hill, New York Monroe D, Hoffman M, Roberts H (2010) Molecular biology and biochemistry of the coagulation factors and pathways of hemostasis. In: Prchal J, Kaushansky K, Lichtman M, Kipps T, Seligsohn U (eds) Williams hematology, 8th edn. McGraw-Hill, New York
go back to reference Mourey L, Samama J, Delarue M, Choay J, Lormeau J, Petitou M, Moras D (1990) Antithrombin III: structural and functional aspects. Biochimie 72(8):599–608PubMedCrossRef Mourey L, Samama J, Delarue M, Choay J, Lormeau J, Petitou M, Moras D (1990) Antithrombin III: structural and functional aspects. Biochimie 72(8):599–608PubMedCrossRef
go back to reference Müller I, Klocke A, Alex M, Kotzsch M, Luther T, Morgenstern E, Zieseniss S, Zahler S, Preissner K, Engelmann B (2003) Intravascular tissue factor initiates coagulation via circulating microvesicles and platelets. FASEB J 17(3):476–478. doi:10.1096/fj.02-0574fje PubMed Müller I, Klocke A, Alex M, Kotzsch M, Luther T, Morgenstern E, Zieseniss S, Zahler S, Preissner K, Engelmann B (2003) Intravascular tissue factor initiates coagulation via circulating microvesicles and platelets. FASEB J 17(3):476–478. doi:10.​1096/​fj.​02-0574fje PubMed
go back to reference Muralidharan-Chari V, Clancy JW, Sedgwick A, D’Souza-Schorey C (2010) Microvesicles: mediators of extracellular communication during cancer progression. J Cell Sci 123(10):1603–1611. doi:10.1242/jcs.064386 PubMedCrossRef Muralidharan-Chari V, Clancy JW, Sedgwick A, D’Souza-Schorey C (2010) Microvesicles: mediators of extracellular communication during cancer progression. J Cell Sci 123(10):1603–1611. doi:10.​1242/​jcs.​064386 PubMedCrossRef
go back to reference Polgar J, Matuskova J, Wagner D (2005) The P-selectin, tissue factor, coagulation triad. J Thromb Haemost 3(8):1590–1596PubMedCrossRef Polgar J, Matuskova J, Wagner D (2005) The P-selectin, tissue factor, coagulation triad. J Thromb Haemost 3(8):1590–1596PubMedCrossRef
go back to reference Rickles FR (2006) Mechanisms of cancer-induced thrombosis in cancer. Pathophysiol Haemost Thromb 35(1–2):103–110PubMedCrossRef Rickles FR (2006) Mechanisms of cancer-induced thrombosis in cancer. Pathophysiol Haemost Thromb 35(1–2):103–110PubMedCrossRef
go back to reference Sawada M, Miyake S, Ohdama S, Matsubara O, Masuda S, Yakumaru K, Yoshizawa Y (1999) Expression of tissue factor in non-small-cell lung cancers and its relationship to metastasis. Br J Cancer 79(3/4):472PubMedCentralPubMedCrossRef Sawada M, Miyake S, Ohdama S, Matsubara O, Masuda S, Yakumaru K, Yoshizawa Y (1999) Expression of tissue factor in non-small-cell lung cancers and its relationship to metastasis. Br J Cancer 79(3/4):472PubMedCentralPubMedCrossRef
go back to reference Seitz R, Heidtmann H–H, Wolf M, Immel A, Egbring R (1997) Prognostic impact of an activation of coagulation in lung cancer. Ann Oncol 8(8):781–784PubMedCrossRef Seitz R, Heidtmann H–H, Wolf M, Immel A, Egbring R (1997) Prognostic impact of an activation of coagulation in lung cancer. Ann Oncol 8(8):781–784PubMedCrossRef
go back to reference Versteeg HH, Spek CA, Peppelenbosch MP, Richel DJ (2004) Tissue factor and cancer metastasis: the role of intracellular and extracellular signaling pathways. Mol Med 10(1–6):6PubMedCentralPubMed Versteeg HH, Spek CA, Peppelenbosch MP, Richel DJ (2004) Tissue factor and cancer metastasis: the role of intracellular and extracellular signaling pathways. Mol Med 10(1–6):6PubMedCentralPubMed
go back to reference Versteeg HH, Heemskerk JW, Levi M, Reitsma PH (2013) New fundamentals in hemostasis. Physiol Rev 93(1):327–358PubMedCrossRef Versteeg HH, Heemskerk JW, Levi M, Reitsma PH (2013) New fundamentals in hemostasis. Physiol Rev 93(1):327–358PubMedCrossRef
Metadata
Title
Elevated circulating levels of tissue factor-positive microvesicles are associated with distant metastasis in lung cancer
Authors
Jo-Chi Tseng
Liang-Che Chang
Boy-Yiing Jiang
Yu-Chih Liu
Hung-Jie Chen
Chih-Teng Yu
Chung-Ching Hua
Publication date
01-01-2014
Publisher
Springer Berlin Heidelberg
Published in
Journal of Cancer Research and Clinical Oncology / Issue 1/2014
Print ISSN: 0171-5216
Electronic ISSN: 1432-1335
DOI
https://doi.org/10.1007/s00432-013-1544-8

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