Clinical significance of procoagulant microparticles

Shosaku Nomura, Michiomi Shimizu, Shosaku Nomura, Michiomi Shimizu

Abstract

Microparticles (MPs) are small membrane vesicles that are released from many different cell types by exocytic budding of the plasma membrane in response to cellular activation or apoptosis. MPs may also be involved in clinical diseases because they express phospholipids, which function as procoagulants. Although flow cytometry is the most widely used method for studying MPs, some novel assays, such as tissue factor-dependent procoagulant assay or the ELISA method, have been reported. However, the use of quantification of MP as a clinical tool is still controversial. Elevated platelet-derived MP, endothelial cell-derived MP, and monocyte-derived MP concentrations are documented in almost all thrombotic diseases occurring in venous and arterial beds. However, the significance of MPs in various clinical conditions remains controversial. An example of this controversy is that it is unknown if MPs found in peripheral blood vessels cause thrombosis or whether they are the result of thrombosis. Numerous studies have shown that not only the quantity, but also the cellular origin and composition of circulating MPs, are dependent on the type of disease, the disease state, and medical treatment. Additionally, many different functions have been attributed to MPs. Therefore, the number and type of clinical disorders associated with elevated MPs are currently increasing. However, MPs were initially thought to be small particles with procoagulant activity. Taken together, our review suggests that MPs may be a useful biomarker to identify thrombosis.

Keywords: Flow cytometry; Microparticle; Phospholipid; Procoagulant activity; Thrombosis.

Figures

Figure 1
Figure 1
Mechanisms participating in the regulation of transmembrane migration of phosphatidylserine (PS) in activated platelets, followed by PDMP shedding. Phospholipid asymmetry is under the control of active flippase, while floppase and scramblase remain inactive. Following cellular activation, calcium is released from the endoplasmic reticulum, which can lead to the loss of phospholipid asymmetry and activation of calpain. PC, phosphatidylcholine; SM, sphingomyeline; PEa, phosphatidylethanolamine.
Figure 2
Figure 2
Different types of secreted membrane microparticles. Microparticles or pre-microparticles originally exist in multivesicular bodies. Following cellular activation, multivesicular bodies move close to the cellular membrane. Microparticles that are generated in multivesicular bodies are called exosomes once they are secreted. Secreted vesicles can form inside internal compartments from where they are subsequently secreted by fusion of these compartments with the plasma membrane. This microparticle is called an ectosome. Active calpain cleaves the cytoskeleton, leading to the formation of a membrane bleb and ectosome release. Exosome functionates by delivery system of some cellular substances. Ectosome possesses a procoagulant activity.
Figure 3
Figure 3
Role of MPs in type 2 diabetes into atherosclerosis and thrombosis. Production of PDMPs, MDMPs, and EDMPs can be increased in type 2 diabetes. These MPs contribute to the generation of atherothrombosis in type 2 diabetes. Mac-1: β-2 integrin family in monocyte (CD11b/CD18), ICAM-1: intercellular adhesion molecule-1, VCAM-1: vascular cell adhesion molecule-1.
Figure 4
Figure 4
Role of TF on MPs in activation of target cells. MPs can carry some substances, such as integrin, cell adhesion molecule, chemokines, phospholipids, and TF. TF mainly contributes to activation of the extrinsic coagulation system. PS, phosphatidylserine; CAM, cell adhesion molecule.

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    1. Nomura S, Shouzu A, Omoto S, Nishikawa M, Iwasaka T. Long-term treatment with nifedipine modulates procoagulant markers and C-C chemokine in hypertensive patients with type 2 diabetes mellitus. Thromb Res. 2005;115:277–285.
    1. Nomura S, Shouzu A, Omoto S, Nishikawa M, Fukuhara S, Iwasaka T. Effects of valsartan on monocyte/endothelial cell activation markers and adiponectin in hypertensive patients with type 2 diabetes mellitus. Thromb Res. 2006;117:385–392.
    1. Nomura S, Inami N, Kimura Y, Omoto S, Shouzu A, Nishikawa M, Iwasaka T. Effect of nifedipine on adiponectin in hypertensive patients with type 2 diabetes mellitus. J Hum Hypertens. 2007;21:38–44.
    1. Ogata N, Nomura S, Shouzu A, Imaizumi M, Arichi M, Matsumura M. Elevation of monocyte-derived microparticles in patients with diabetic retinopathy. Diabetes Res Clin Pract. 2006;73:241–248.
    1. Koga H, Sugiyama SD, Kugiyama K, Watanabe K, Fukushima H, Tanaka T, Sakamoto T, Yoshimura M, Jinnouchi H, Ogawa H. Elevated levels of VE-cadherin-positive endothelial microparticles in patients with type 2 diabetes mellitus and coronary artery disease. J Am Coll Cardiol. 2005;45:1622–1630.
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    1. Hatada T, Wada H, Nobori T, Okabayashi K, Maruyama K, Abe Y, Uemoto S, Yamada S, Maruyama I. Plasma concentrations and importance of High Mobility Group Box protein in the prognosis of organ failure in patients with disseminated intravascular coagulation. Thromb Haemost. 2005;94:975–979.
    1. Nomura S, Fujita S, Ozasa R, Nakanishi T, Miyaji M, Mori S, Ito T, Ishii K. Correlation between platelet activation markers and HMGB1 in DIC patients with hematologic malignancy. Platelets. 2011;22:396–397.
    1. Delabrache X, Boisramé-Helms J, Asfar P, Berger A, Mootien Y, Lavigne T, Grunebaum L, Lanza F, Gachet C, Freyssinet JM, Toti F, Meziani F. Microparticles are new biomarkers of septic shock-induced disseminated intravascular coagulopathy. Intensive Care Med. 2013;39:1695–1703.
    1. Hellum M, Øvstebø R, Brusletto BS, Berg JP, Brandtzaeg P, Henriksson CE. Microparticle-associated tissue factor activity correlates with plasma levels of bacterial lipopolysaccharides in meningococcal septic shock. Thromb Res. 2014;133:507–514.
    1. Nomura S, Kagawa H, Ozaki Y, Nagahama M, Yoshimura C, Fukuhara S. Relationship between platelet activation and cytokines in systemic inflammatory response syndrome patients with hematological malignancies. Thromb Res. 1999;95:205–213.
    1. Nieuwland R, Berckmans RJ, McGregor S, Böing AN, Romijin FP, Westendorp RG, Hack CE, Sturk A. Cellular origin and procoagulant properties of microparticles in meningococcal sepsis. Blood. 2000;95:930–935.
    1. Nomura S, Inami N, Kanazawa S, Iwasaka T, Fukuhara S. Elevation of platelet activation markers and chemokines during peripheral blood stem cell harvest with G-CSF. Stem Cells. 2004;22:696–703.
    1. Nomura S, Ishii K, Inami N, Kimura Y, Uoshima N, Urase F, Maeda Y, Hayashi K. α4 integrin-positive microvesicles and SDF-1 in peripheral blood stem cell harvest. Bone Marrow Transplant. 2008;41:1071–1072.
    1. Nomura S, Ishii K, Inami N, Kimura Y, Uoshima N, Ishida H, Yoshihara T, Urase F, Maeda Y, Hayashi K. Evaluation of angiopoietin and cell-derived microparticles after stem cell transplantation. Biol Blood Marrow Transplant. 2008;14:766–774.
    1. Nomura S, Inami N, Ozaki Y, Kagawa H, Fukuhara S. Significance of microparticles in progressive systemic sclerosis with interstitial pneumonia. Platelets. 2008;19:192–198.
    1. Nomura S, Imamura A, Okuno M, Kamiyama Y, Fujimura Y, Ikeda Y, Fukuhara S. Platelet-derived microparticles in patients with arteriosclerosis obliterans: enhancement of high shear-induced microparticle generation by cytokines. Thromb Res. 2000;98:257–268.
    1. Nomura S, Inami N, Iwasaka T, Liu Y. Platelet activation marker, microparticles and soluble adhesion molecules are elevated in patients with atherosclerosis obliterans: therapeutic effects by cilostazol and potentiation by dipyridamole. Platelets. 2004;15:167–172.
    1. Nomura S, Shouzu Omoto S, Nishikawa M, Iwasaka T. 5-HT2A receptor antagonist increases circulating adiponectin in patients with type 2 diabetes mellitus. Blood Coagul Fibrinolysis. 2005;16:423–428.
    1. Baj-Kizyworzeka M, Majka M, Oratico D, Ratajczak J, Vilaire G, Kijowski J, Reca R, Janowska-Wieczorek A, Ratajczak MZ. Platelet-derived microparticles stimulate proliferation, survival, adhesion, and chemotaxis of hematopoietic cells. Exp Hematol. 2002;30:450–459.
    1. Nomura S, Kanazawa S, Inami N, Kamitsuji Y, Uoshima N, Ishida H, Yoshihara T, Kitayama H, Hayashi K. Role of platelet-derived chemokines (RANTES and ENA-78) after stem cell transplantation. Transpl Immunol. 2006;15:247–253.
    1. Nomura S, Ishii K, Inami N, Uoshima N, Ishida H, Yoshihara T, Kitayama H, Hayashi K. Role of soluble tumor necrosis factor-related apoptosis-inducing ligand concentration after stem cell transplantation. Transpl Immunol. 2007;18:115–121.
    1. Majka M, Kijowski J, Lesko E, Gozdzik J, Zupanska B, Ratajczak MZ. Evidence that platelet-derived microvesicles may transfer platelet-specific immunoreactive antigens to the surface of endothelial cells and CD34+ hematopoietic stem/progenitor cells – implication for the pathogenesis of immune thrombocytopenias. Folia Histochem Cytobiol. 2007;45:27–32.
    1. Deregibus MC, Cantaluppi V, Calogero R, Lo Iacono M, Tetta C, Biancone L, Bruno S, Bussolati B, Camussi G. Endothelial progenitor cell-derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood. 2007;110:2440–2448.
    1. Janowska-Wieczorek A, Wysoczynski M, Kijowski J, Marquez-Curtis L, Machalinski B, Ratajczak J, Ratajczak MZ. Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer. Int J Cancer. 2005;113:752–760.
    1. Ratajczak J, Miekus K, Kucia M, Zhang J, Reca R, Dvorak P, Ratajczak MZ. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia. 2006;20:847–856.
    1. Kanazawa S, Nomura S, Kuwana M, Muramatsu M, Yamaguchi K, Fukuhara S. Monocyte-derived microparticles may be a sign of vascular complication in patients with lung cancer. Lung Cancer. 2003;39:145–149.
    1. 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.
    1. Kalinkovich A, Tavor S, Avigdor A, Kahn J, Brill A, Petit I, Goichberg P, Tesio M, Netzer N, Naparstek E, Hardan I, Nagler A, Resnick I, Tsimanis A, Lapidot T. Functional CXCR4-expressing microparticles and SDF-1 correlate with circulating acute myelogenous leukemia cells. Cancer Res. 2006;66:11013–11020.
    1. Yu JL, May L, Lhotak V, Shahrzad S, Shirasawa S, Weitz JI, Coomber BL, Mackman N, Rak JW. Oncogenic events regulate tissue factor expression in colorectal cancer cells: implications for tumor progression and angiogenesis. Blood. 2005;105:1734–1741.
    1. DelConde I, Bharwani LD, Dietzen DJ, Pendurthi U, Thiagarajan P, Lopez JA. Microvesicle-associated tissue factor and Trousseau's syndrome. J Thromb Haemost. 2007;5:70–74.
    1. 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.
    1. Tilley RE, Holscher T, Belani R, Nieva J, Mackman N. Tissue factor activity is increased in a combined platelet and microparticle sample from cancer patients. Thromb Res. 2008;122:604–609.
    1. Davila M, Amirkhosravi A, Coll E, Desai H, Robles L, Colon J, Baker CH, Francis JL. Tissue factor-bearing microparticles derived from tumor cells: impact on coagulation activation. J Thromb Haemost. 2008;6:1517–1524.
    1. Meng Y, Kang S, Fishman DA. Lysophosphatidic acid stimulates Fas ligand microvesicles release from ovarian cancer cells. Cancer Immunol Immunother. 2005;54:807–814.
    1. Kim JW, Wieckowski E, Taylor DD, Reichert TE, Watkins S, Whiteside TL. Fas ligand-positive membranous vesicles isolated from sera of patients with oral cancer induce apoptosis of activated T lymphocytes. Clin Cancer Res. 2005;11:1010–1020.
    1. Huber V, Fais S, Iero M, Lugini L, Canese P, Squarcina P, Zaccheddu A, Colone M, Arancia G, Gentile M, Seregni E, Valenti R, Ballabio G, Belli F, Leo E, Parmiani G, Rivoltini L. Human colorectal cancer cells induce T-cell death through release of proapoptotic microvesicles: role in immune escape. Gastroenterology. 2005;128:1796–1804.
    1. Morel O, Ohlmann P, Epailly E, Backouboula B, Zobairi F, Jesel L, Meyer N, Chenard MP, Freyssinet JM, Bareiss P, Mazzucotelli JP, Toti F. Endothelial cell activation contributes to the release of procoagulant microparticles during acute cardiac allograft rejection. J Heart Lung Transplant. 2008;27:38–45.
    1. Bakouboula B, Morel O, Faure A, Zobairi F, Jesel L, Trinh A, Zupan M, Canuet M, Grunebaum L, Brunette A, Desprez D, Chabot F, Weitzenblum E, Freyssinet JM, Chaouat A, Toti F. Procoagulant membrane microparticles correlate with the severity of pulmonary arterial hypertension. Am J Respir Crit Care Med. 2008;177:536–543.

Source: PubMed

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