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Journal of Cancer Research and Clinical Oncology

Erschienen in:

01.01.2014 | Original Paper

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

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

Erschienen in: Journal of Cancer Research and Clinical Oncology | Ausgabe 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.

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

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

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

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

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

Carmeliet P, Collen D (2000) Molecular basis of angiogenesis: role of VEGF and VE-cadherin. Ann NY Acad Sci 902(1):249–264. doi:10.1111/j.1749-6632.2000.tb06320.x PubMedCrossRef

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

de Groot PG, Urbanus RT, Roest M (2012) Platelet interaction with the vessel wall. Handb Exp Pharmacol 210:87–110. doi:10.1007/978-3-642-29423-5_4 PubMedCrossRef

Fidler IJ (2003) The pathogenesis of cancer metastasis: the ‘seed and soil’ hypothesis revisited. Nat Rev Cancer 3(6):453–458PubMedCrossRef

Fleitas T, Martinez-Sales V, Vila V, Reganon E, Mesado D, Martin M, Gomez-Codina J, Montalar J, Reynes G (2012) Circulating endothelial cells and microparticles as prognostic markers in advanced non-small cell lung cancer. PLoS ONE 7(10):e47365. doi:10.1371/journal.pone.0047365 PubMedCentralPubMedCrossRef

Gay LJ, Felding-Habermann B (2011) Contribution of platelets to tumour metastasis. Nat Rev Cancer 11(2):123–134PubMedCrossRef

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

Hicklin DJ, Ellis LM (2005) Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J Clin Oncol 23(5):1011–1027. doi:10.1200/jco.2005.06.081 PubMedCrossRef

Hood JL, San RS, Wickline SA (2011) Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res 71(11):3792–3801. doi:10.1158/0008-5472.can-10-4455 PubMedCrossRef

Horstman LL, Ahn YS (1999) Platelet microparticles: a wide-angle perspective. Crit Rev Oncol Hematol 30(2):111–142. doi:10.1016/S1040-8428(98)00044-4 PubMedCrossRef

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

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

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

Lee AY (2002) Cancer and thromboembolic disease: pathogenic mechanisms. Cancer Treat Rev 28(3):137–140. doi:10.1016/S0305-7372(02)00044-0 PubMedCrossRef

Martin T, Mason M, Jiang W (2011) Tight junctions in cancer metastasis. Front Biosci 16:898CrossRef

Mause SF, Weber C (2010) Microparticles: protagonists of a novel communication network for intercellular information exchange. Circ Res 107(9):1047–1057. doi:10.1161/circresaha.110.226456 PubMedCrossRef

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

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

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

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

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

Nierodzik ML, Karpatkin S (2006) Thrombin induces tumor growth, metastasis, and angiogenesis: evidence for a thrombin-regulated dormant tumor phenotype. Cancer Cell 10(5):355–362. doi:10.1016/j.ccr.2006.10.002 PubMedCrossRef

Piccin A, Murphy WG, Smith OP (2007) Circulating microparticles: pathophysiology and clinical implications. Blood Rev 21(3):157–171. doi:10.1016/j.blre.2006.09.001 PubMedCrossRef

Polgar J, Matuskova J, Wagner D (2005) The P-selectin, tissue factor, coagulation triad. J Thromb Haemost 3(8):1590–1596PubMedCrossRef

Rickles FR (2006) Mechanisms of cancer-induced thrombosis in cancer. Pathophysiol Haemost Thromb 35(1–2):103–110PubMedCrossRef

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

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

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, Heemskerk JW, Levi M, Reitsma PH (2013) New fundamentals in hemostasis. Physiol Rev 93(1):327–358PubMedCrossRef

Vestweber D (2008) VE-cadherin: the major endothelial adhesion molecule controlling cellular junctions and blood vessel formation. Arterioscler Thromb Vasc Biol 28(2):223–232. doi:10.1161/atvbaha.107.158014 PubMedCrossRef

Weis S, Cui J, Barnes L, Cheresh D (2004) Endothelial barrier disruption by VEGF-mediated Src activity potentiates tumor cell extravasation and metastasis. J Cell Biol 167(2):223–229. doi:10.1083/jcb.200408130 PubMedCrossRef

Wysoczynski M, Ratajczak MZ (2009) Lung cancer secreted microvesicles: underappreciated modulators of microenvironment in expanding tumors. Int J Cancer 125(7):1595–1603. doi:10.1002/ijc.24479 PubMedCentralPubMedCrossRef

Titel: Elevated circulating levels of tissue factor-positive microvesicles are associated with distant metastasis in lung cancer
verfasst von: Jo-Chi Tseng
Liang-Che Chang
Boy-Yiing Jiang
Yu-Chih Liu
Hung-Jie Chen
Chih-Teng Yu
Chung-Ching Hua
Publikationsdatum: 01.01.2014
Verlag: Springer Berlin Heidelberg
Erschienen in: Journal of Cancer Research and Clinical Oncology / Ausgabe 1/2014
Print ISSN: 0171-5216
Elektronische ISSN: 1432-1335
DOI: https://doi.org/10.1007/s00432-013-1544-8

Springer Medizin

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