Microvesicles in Health and Disease

Archivum Immunologiae et Therapiae Experimentalis - Tập 60 - Trang 107-121 - 2012
Jameel M. Inal1, Ephraim A. Ansa-Addo1, Dan Stratton1, Sharad Kholia1, Samuel S. Antwi-Baffour1, Samireh Jorfi1, Sigrun Lange2
1Cellular and Molecular Immunology Research Centre, Faculty of Life Sciences, London Metropolitan University, London, UK
2Perinatal Brain Repair Group, Institute for Women’s Health, University College London, London, UK

Tóm tắt

Microvesicles (or MVs) are plasma membrane-derived vesicles released from most eukaryotic cells constitutively during early apoptosis or at higher levels after chemical or physical stress conditions. This review looks at some of the functions of MVs in terms of intercellular communication and ensuant signal transduction, including the transport of proteins (unconventional protein export) as well as of mRNA and microRNA. MVs also have roles in membrane repair, the removal of misfolded proteins, and in the control of apoptosis. We also discuss the role MVs have been shown to have in invasive growth and metastasis as well as in hypoxia in tumours and cerebral ischaemia. The association of MVs in infectious and autoimmune disease is also summarised together with their possible use as therapeutic agents.

Tài liệu tham khảo

Abid Hussein MN, Böing AN, Sturk A et al (2007) Inhibition of microparticle release triggers endothelial cell apoptosis and detachment. Thromb Haemost 98:1096–1107 Abrahams VM, Straszewski-Chavez SL, Guller S (2004) First trimester trophoblast cells secrete Fas ligand which induces immune cell apoptosis. Mol Hum Reprod 10:55–63 Albert ML, Kim JI, Birge RB (2000) Alphavbeta5 intregrin recruits the crkII-Dock180-rac1 complex for phagocytosis of apoptotic cells. Nat Cell Biol 2:899–905 Alvarez-Erviti L, Seow Y, Yin H et al (2011) Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol 29:341–345 Amabile N, Heiss C, Real WM et al (2008) Circulating endothelial microparticle levels predict hemodynamic severity of pulmonary hypertension. Am J Respir Crit Care Med 177:1268–1275 Andreola G, Rivoltini L, Castelli C et al (2002) Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing microvesicles. J Exp Med 195:1303–1316 Ansa-Addo EA, Lange S, Stratton D et al (2010) Human plasma membrane-derived vesicles halt proliferation and induce differentiation of THP-1 acute monocytic leukaemia cells. J Immunol 185:5236–5246 Ansa-Addo EA, Cestari I, Pathak P et al (2012) Trypanosoma cruzi utilisation of host cell microvesicle release aids invasion. J Immunol (submitted) Antonyak MA, Li B, Boroughs LK et al (2011) Cancer cell-derived microvesicles induce transformation by transferring tissue transglutaminase and fibronectin to recipient cells. Proc Natl Acad Sci USA 108:4852–4857 Antwi-Baffour S, Kholia S, Aryee YK-D et al (2010) Human plasma membrane-derived vesicles inhibit the phagocytosis of apoptotic cells—possible role in SLE. Biochem Biophys Res Commun 398:278–283 Aoki N, Yokoyama R, Asai N et al (2010) Adipocyte-derived microvesicles are associated with multiple angiogenic factors and induce angiogenesis in vivo and in vitro. Endocrinology 151:2567–2576 Baj-Krzyworzeka M, Majka M, Pratico D et al (2002) Platelet-derived microparticles stimulate proliferation, survival, adhesion, and chemotaxis of hematopoietic cells. Exp Hematol 30:450–459 Baj-Krzyworzeka M, Szatanek R, Weglarczyk K et al (2006) Tumour-derived microvesicles carry several surface determinants and mRNA of tumour cells and transfer some of these determinants to monocytes. Cancer Immunol Immunother 55:808–818 Baj-Krzyworzeka M, Szatanek R, Weglarczyk K et al (2007) Tumour-derived microvesicles modulate biological activity of human monocytes. Immunol Lett 113:76–82 Barry OP, Kazanietz MG, Pratico D et al (1999) Arachidonic acid in platelet microparticles up-regulates cyclooxygenase-2-dependent prostaglandin formation via a protein kinase C/mitogen-activated protein kinase-dependent pathway. J Biol Chem 274:7545–7556 Barry OP, Pratico D, Savani RC et al (1998) Modulation of monocyte-endothelial cell interactions by platelet microparticles. J Clin Invest 102:136–144 Basse F, Gaffet P, Bienvenue A (1994) Correlation between inhibition of cytoskeleton proteolysis and anti-vesiculation effect of calpeptin during A23187-induced activation of human platelets: are vesicles shed by filopod fragmentation? Biochim Biophys Acta 1190:217–224 Berger EA, Murphy PM, Farber JM (1999) Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. Annu Rev Immunol 17:657–700 Bess JW Jr, Gorelic RJ, Bosche WJ et al (1997) Microvesicles are a source of contaminating cellular proteins found in purified HIV-1 preparations. Virology 230:134–144 Bevers EM, Comfurius P, van Rijn JL et al (1982) Generation of prothrombin-converting activity and the exposure of phosphatidylserine at the outer surface of platelets. Eur J Biochem 122:429–436 Böing N, Hau CM, Sturk A et al (2008) Platelet microparticles contain active caspase 3. Platelets 19:96–103 Bombara C, Ignotz RA (1992) TGF-beta inhibits proliferation of and promotes differentiation of human promonocytic leukemia cells. J Cell Physiol 153:30–37 Borisenko GG, Matsura T, Liu SX et al (2003) Macrophage recognition of externalized phosphatidylserine and phagocytosis of apoptotic Jurkat cells—existence of a threshold. Arch Biochem Biophys 413:41–52 Bratton DL, Fadok VA, Richter DA et al (1997) Appearance of phosphatidylserine on apoptotic cells requires calcium-mediated nonspecific flip-flop and is enhanced by loss of the aminophospholipid translocase. J Biol Chem 272:26159–26165 Brechot N, Gomez E, Bignon M et al (2008) Modulation of macrophage activation state protects tissue from necrosis during critical limb ischemia in thrombospondin-1-deficient mice. PLoS One 3:e3950 Brüne B (2003) Nitric oxide: NO apoptosis or turning it ON? Cell Death Differ 10:864–869 Butikofer P, Kuypers FA, Xu CM et al (1989) Enrichment of two glycosylphosphatidylinositol-anchored proteins, acetylcholinesterase and decay accelerating factor, in vesicles released from human red blood cells. Blood 74:1481–1485 Cestari I, Ansa-Addo E, Deolindo P et al (2012) Trypanosoma cruzi immune evasion mediated by host cell-derived microvesicles. J Immunol 188:1942–1952 Chargaff E, West R (1946) The biological significance of the thromboplastic protein of blood. J Biol Chem 166:189–197 Chen JF, Goeddel DV (2002) TNF-R1 signaling: a beautiful pathway. Science 296:1634–1635 Cheng EH, Sheiko TV, Fisher JK et al (2003) VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 301:513–517 Cherian P, Hankey GJ, Eikelboom JW et al (2003) Endothelial and platelet activation in acute ischemic stroke and its etiological subtypes. Stroke 34:2132–2137 Chiarugi A, Moskowitz MA (2002) Cell biology. PARP-1—a perpetrator of apoptotic cell death? Science 297:200–201; comments 259–263 Cleves AE (1997) Protein transports: the nonclassical ins and outs. Curr Biol 7:R318–R320 Cohen JJ, Duke RC, Fadok VA et al (1992) Apoptosis and programmed cell death in immunity. Annu Rev Immunol 10:267–293 Combes V, Coltel N, Alibert M et al (2005) ABCA1 gene deletion protects against cerebral malaria: potential pathogenic role of microparticles in neuropathology. Am J Pathol 166:295–302 Del Conde I, Shrimpton CN, Thiagarajan P et al (2005) Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood 106:1604–1611 Deregibus MC, Cantaluppi V, Calogero R et al (2007) Endothelial progenitor cell-derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood 110:2440–2448 Distler JH, Pisetsky DS, Huber LC et al (2005) Microparticles as regulators of inflammation: novel players of cellular crosstalk in the rheumatic diseases. Arthritis Rheum 52:3337–3348 Do JT, Schöler HR (2004) Nuclei of embryonic stem cells reprogram somatic cells. Stem Cells 22:941–949 Edinger AL, Mankowski JL, Doranz BJ et al (1997) CD4-independent, CCR5-dependent infection of brain capillary endothelial cells by a neurovirulent simian immunodeficiency virus strain. Proc Natl Acad Sci USA 94:14742–14747 Eugenin EA, Morgello S, Klotman ME et al (2008) Human immunodeficiency virus (HIV) infects human arterial smooth muscle cells in vivo and in vitro: implications for the pathogenesis of HIV-mediated vascular disease. Am J Pathol 172:1100–1111 Fadok VA, Bratton DL, Konowal A et al (1998) Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J Clin Invest 101:890–898 Fauci AS (1996) Host factors and the pathogenesis of HIV-induced disease. Nature 384:529–534 Florkiewicz RZ, Majack RA, Buechler RD et al (1995) Quantitative export of FGF-2 occurs through an alternative, energy-dependent, non-ER/Golgi pathway. J Cell Physiol 162:388–399 Fox JE, Austin CD, Boyles JK et al (1990) Role of the membrane skeleton in preventing the shedding of procoagulant-rich microvesicles from the platelet plasma membrane. J Cell Biol 111:483–493 Freyssinet JM (2003) Cellular microparticles: what are they bad or good for? J Thromb Haemost 1:1655–1662 Friend C, Marovitz W, Henie G et al (1978) Observations on cell lines derived from a patient with Hodgkin’s disease. Cancer Res 38:2581–2591 Fritzsching B, Schwer B, Kartenbeck J et al (2002) Release and intercellular transfer of cell surface CD81 via microparticles. J Immunol 169:5531–5537 Furie B, Furie BC (2004) Role of platelet P-selectin and microparticle PSGL-1 in thrombus formation. Trends Mol Med 10:171–178 Gasser O, Hess C, Miot S et al (2003) Characterisation and properties of ectosomes released by human polymorphonuclear neutrophils. Exp Cell Res 285:243–257 Gasser O, Schifferli JA (2004) Activated polymorphonuclear neutrophils disseminate anti-inflammatory microparticles by ectocytosis. Blood 104:2543–2548 Gaustad KG, Boquest AC, Anderson BE (2004) Differentiation of human adipose tissue stem cells using extracts of rat cardiomyocytes. Biochem Biophys Res Commun 314:420–427 George JN, Thoi LL, McManus LM et al (1982) Isolation of human platelet membrane microparticles from plasma and serum. Blood 60:834–840 Ginestra A, La Placa MD, Saladino F et al (1998) The amount and proteolytic content of vesicles shed by human cancer cell lines correlates with their in vitro invasiveness. Anticancer Res 18:3433–3437 Gould SJ, Booth AM, Hildreth JE (2003) The Trojan exosome hypothesis. Proc Natl Acad Sci USA 100:10592–10597 Grange C, Tapparo M, Collino F et al (2011) Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res 71:5346–5356 Grant R, Ansa-Addo EA, Stratton D et al (2011) A filtration-based protocol to isolate human plasma membrane-derived vesicles and exosomes from blood plasma. J Immunol Methods 371:143–151 Graves LE, Ariztia EV, Navari JR et al (2004) Proinvasive properties of ovarian cancer ascites-derived membrane vesicles. Cancer Res 64:7045–7049 Hakulinen J, Junnikkala S, Sorsa T et al (2004) Complement inhibitor membrane cofactor protein (MCP; CD46) is constitutively shed from cancer cell membranes in vesicles and converted by a metalloproteinase to a functionally active soluble form. Eur J Immunol 34:2620–2629 Halder SK, Beauchamp RD, Datta PK (2005) A specific inhibitor of TGF-beta receptor kinase, SB-431542, as a potent antitumor agent for human cancers. Neoplasia 7:509–521 Hamilton KK, Hattori R, Esmon CT et al (1990) Complement proteins C5b-9 induce vesiculation of the endothelial plasma membrane and expose catalytic surface for assembly of the prothrombinase enzyme complex. J Biol Chem 265:3809–3814 Hansen WR, Fletcher DA (2008) Tonic shock induces detachment of Giardia lamblia. PloS Negl Trop Dis 2:e169 Herrmann M, Voll RE, Zoller OM et al (1998) Impaired phagocytosis of apoptotic cell material by monocyte derived macrophages from patients with systemic lupus erythematosus. Arthritis Rheum 41:1241–1250 Hess C, Sadallah S, Hefti A et al (1999) Ectosomes released by human neutrophils are specialized functional units. J Immunol 163:4564–4573 Hind E, Heugh S, Ansa-Addo EA et al (2010) Red cell PMVs, plasma membrane-derived vesicles calling out for standards. Biochem Biophys Res Commun 399:465–469 Hochedlinger K, Plath K (2009) Epigenetic reprogramming and induced pluripotency. Development 136:509–523 Horstman LL, Ahn YS (1999) Platelet microparticles: a wide-angle perspective. Crit Rev Oncol Hematol 30:111–142 Hsu HH, Camacho NP (1999) Isolation of calcifiable vesicles from human atherosclerotic aortas. Atherosclerosis 143:353–362 Huber V, Fais S, Iero M et al (2005) Human colorectal cancer cells induce T-cell death through release of proapoptotic microvesicles: role in immune escape. Gastroenterology 128:1796–1804 Hugel B, Martinez MC, Kunzelmann C et al (2005) Membrane microparticles: two sides of the coin. Physiology 20:22–27 Hughes RC (1999) Secretion of the galectin family of mammalian carbohydrate-binding proteins. Biochim Biophys Acta 1473:172–185 Jacobson K, Dietrich C (1999) Looking at lipid rafts? Trends Cell Biol 9:87–91 Janowska-Wieczorek A, Majka M, Kijowski J et al (2001) Platelet-derived microparticles bind to hematopoietic stem/progenitor cells and enhance their engraftment. Blood 98:3143–3149 Janowska-Wieczorek A, Marquez-Curtis LA, Wysoczynski M et al (2006) Enhancing effect of platelet-derived microvesicles on the invasive potential of breast cancer cells. Transfusion 46:1199–1209 Janowska-Wieczorek A, Wysoczynski M, Kijowski J et al (2005) Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer. Int J Cancer 113:752–760 Jy W, Jimenez JJ, Mauro LM et al (2002) Agonist-induced capping of adhesion proteins and microparticle shedding in cultures of human renal microvascular endothelial cells. Endothelium 9:179–189 Kelton JG, Warkentin TE, Hayward CP et al (1992) Calpain activity in patients with thrombotic thrombocytopenic purpura is associated with platelet microparticles. Blood 80:2246–2251 Khiati A, Chaloin O, Muller S et al (2010) Induction of monocyte chemoattractant protein-1 (MCP-1/CCL2) gene expression by human immunodeficiency virus-1 Tat in human astrocytes is CDK9 dependent. J Neurovirol 16:150–167 Kim HK, Song KS, Park YS et al (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 39:184–191 Kim JW, Wieckowski E, Taylor DD et al (2005) Fas ligand-positive membranous vesicles isolated form sera of patients with oral cancer induce apoptosis of activated T lymphocytes. Clin Cancer Res 11:1010–1020 Lee MC, Miller EA, Goldberg J et al (2004) Bi-directional protein transport between the ER and Golgi. Annu Rev Cell Dev Biol 20:87–123 Lima LG, Chammas R, Monteiro RQ et al (2009) Tumor-derived microvesicles modulate the establishment of metastatic melanoma in a phosphatidylserine-dependent manner. Cancer Lett 283:168–175 Lutomski D, Fouillit M, Bourin P et al (1997) Externalization and binding of galectin-1 on cell surface of K562 cells upon erythroid differentiation. Glycobiology 7:1193–1199 Mack M, Kleinschmidt A, Bruhl H et al (2000) Transfer of the chemokine receptor CCR5 between cells by membrane-derived microparticles: a mechanism for cellular human immunodeficiency virus 1 infection. Nat Med 6:769–775 MacKenzie A, Wilson HL, Kiss-Toth E et al (2001) Rapid secretion of interleukin-1beta by microvesicle shedding. Immunity 15:825–835 McNeil PL, Muthukrishnan L, Warder E et al (1989) Growth factors are released by mechanically wounded endothelial cells. J Cell Biol 109:811–822 Maizel A, Tassetto M, Filhol O et al (2002) Engrailed homeoprotein secretion is a regulated process. Development 129:3545–3553 Majka M, Janowska-Wieczorek A, Ratajczak J et al (2001) Numerous growth factors, cytokines, and chemokines are secreted by human CD34(+) cells, myeloblasts, erythroblasts, and megakaryoblasts and regulate normal hematopoiesis in an autocrine/paracrine manner. Blood 97:3075–3085 Majka M, Kijowski J, Lesko E et al (2007) 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 45:27–32 Majka M, Rozmyslowicz T, Honczarenko M et al (2000) Biological significance of the expression of HIV-related chemokine coreceptors (CCR5 and CXCR4) and their ligands by human hematopoietic cell lines. Leukemia 14:1821–1832 Mallat Z, Benamer H, Hugel B et al (2000) Elevated levels of shed membrane microparticles with procoagulant potential in the peripheral circulating blood of patients with acute coronary syndromes. Circulation 101:841–843 Martinez MC, Larbret F, Zobairi F et al (2006) Transfer of differentiation signal by membrane microvesicles harboring hedgehog morphogens. Blood 108:3012–3020 Matzdorff AC, Berchner D, Kuhnel G et al (1998) Relative and absolute changes of activated platelets, microparticles and platelet aggregates after activation in vitro. Haemostasis 28:277–288 Morgan BP, Campbell AK (1985) The recovery of human polymorphonuclear leucocytes from sublytic complement attack is mediated by changes in intracellular free calcium. Biochem J 231:205–208 Mostefai HA, Andriantsitohaina R, Martinez MC (2008) Plasma membrane microparticles in angiogenesis: role in ischemic diseases and in cancer. Physiol Res 57:311–320 Muralidharan-Chari V, Clancy JW, Sedgwick A et al (2010) Microvesicles: mediators of extracellular communication during cancer progression. J Cell Sci 123:1603–1611 Nagai A, Sato T, Akimoto N et al (2005) Isolation and identification of histone H3 protein enriched in microvesicles secreted from cultured sebocytes. Endocrinology 146:2593–2601 Nickel W (2003) The mystery of nonclassical protein secretion. A current view on cargo proteins and potential export routes. Eur J Biochem 270:2109–2119 Nickel W (2005) Unconventional secretory routes: direct protein export across the plasma membrane of mammalian cells. Traffic 6:607–614 Nilsson J, Skog J, Nordstrand A et al (2009) Prostate cancer-derived urine exosomes: a novel approach to biomarkers for prostate cancer. Br J Cancer 100:1603–1607 Niu X, Gupta K, Yang JT et al (2009) Physical transfer of membrane and cytoplasmic components as a general mechanism of cell–cell communication. J Cell Sci 122:600–610 Nolan S, Dixon R, Norman K et al (2008) Nitric oxide regulates neutrophil migration through microparticle formation. Am J Pathol 172:265–273 Omoto S, Nomura S, Shouzu A et al (2002) Detection of monocyte-derived microparticles in patients with Type II diabetes mellitus. Diabetologia 45:550–555 Pap E, Pallinger E, Pasztoi M et al (2009) Highlights of a new type of intercellular communication: microvesicle-based information transfer. Inflamm Res 58:1–8 Park JE, Tan HS, Datta A et al (2010) Hypoxic tumor cell modulates its microenvironment to enhance angiogenic and metastatic potential by secretion of proteins and exosomes. Mol Cell Proteomics 9:1085–1099 Pelchen-Matthews A, Raposo G, Marsh M (2004) Endosomes, exosomes and Trojan viruses. Trends Microbiol 12:310–316 Piccin A, Murphy WG, Smith OP (2007) Circulating microparticles: pathophysiology and clinical implications. Blood Rev 21:157–171 Prudovsky I, Bagala C, Tarantini F et al (2002) The intracellular translocation of the components of the fibroblast growth factor 1 release complex precedes their assembly prior to export. J Cell Biol 158:201–208 Putz U, Howitt J, Lackovic J et al (2008) Nedd4 family-interacting protein 1 (Ndfip1) is required for the exosomal secretion of Nedd4 family proteins. J Biol Chem 283:32621–32627 Qu J, Adam J, Bloxham DM et al (2000) Phosphatidylserine-dependent adhesion of T cells to endothelial cells. Biochim Biophys Acta 1501:99–115 Ratajczak J, Miekus K, Kucia M et al (2006a) Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia 20:847–856 Ratajczak J, Wysoczynski M, Hayek F et al (2006b) Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 20:1487–1495 Rauch U, Antoniak S (2007) Tissue factor-positive microparticles in blood associated with coagulopathy in cancer. Thromb Haemost 97:9–10 Robertson C, Booth SA, Beniac DR et al (2006) Cellular prion protein is released on exosomes from activated platelets. Blood 107:3907–3911 Rood IM, Deegens JK, Merchant ML et al (2010) Comparison of three methods for isolation of urinary microvesicles to identify biomarkers of nephrotic syndrome. Kidney Int 78:810–816 Rubartelli A, Cozzolino F, Talio M et al (1990) A novel secretory pathway for interleukin-1 beta, a protein lacking a signal sequence. EMBO J 9:1503–1510 Sadallah S, Eken C, Schifferli JA (2008) Erythrocyte-derived ectosomes have immunosuppressive properties. J Leukoc Biol 84:1316–1325 Safaei R, Larson BJ, Cheng TC et al (2005) Abnormal lysosomal trafficking and enhanced exosomal export of cisplatin in drug-resistant human ovarian carcinoma cells. Mol Cancer Ther 4:1595–1604 Samson M, Libert F, Doranz BJ et al (1996) Resistance to HIV-1 infection in caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 382:722–725 Sapet C, Simoncini S, Loriod B et al (2006) Thrombin-induced endothelial microparticle generation: identification of a novel pathway involving ROCK-II activation by caspase-2. Blood 108:1868–1876 Sarkar A, Mitra S, Mehta S et al (2009) Monocyte derived microvesicles deliver a cell death message via encapsulated caspase-1. PLoS One 4:e7140 Satta N, Toti F, Feugeas O et al (1994) Monocyte vesiculation is a possible mechanism for dissemination of membrane-associated procoagulant activities and adhesion molecules after stimulation by lipopolysaccharide. J Immunol 153:3245–3255 Scanu A, Molnarfi N, Brandt KJ et al (2008) Stimulated T cells generate microparticles, which mimic cellular contact activation of human monocytes: differential regulation of pro- and anti-inflammatory cytokine production by high-density lipoproteins. J Leukoc Biol 83:921–927 Scholz T, Temmler U, Krause S et al (2002) Transfer of tissue factor from platelets to monocytes: role of platelet-derived microvesicles and CD62P. Thromb Haemost 88:1033–1038 Segerer S, Mack M, Regele H et al (1999) Expression of the C-C chemokine receptor 5 in human kidney diseases. Kidney Int 56:52–64 Shah MD, Bergeron AL, Dong JF et al (2008) Flow cytometric measurement of microparticles: pitfalls and protocol modifications. Platelets 19:365–372 Shedden K, Xie XT, Chandaroy P et al (2003) Expulsion of small molecules in vesicles shed by cancer cells: association with gene expression and chemosensitivity profiles. Cancer Res 63:4331–4337 Shet AS, Aras O, Gupta K et al (2003) Sickle blood contains tissue factor-positive microparticles derived from endothelial cells and monocytes. Blood 102:2678–2683 Simak J, Gelderman MP (2006) Cell membrane microparticles in blood and blood products: potentially pathogenic agents and diagnostic markers. Transfus Med Rev 20:1–26 Simak J, Gelderman MP, Yu H et al (2006) Circulating endothelial microparticles in acute ischemic stroke: a link to severity, lesion volume and outcome. J Thromb Haemost 4:1296–1302 Simak J, Holada K, Vostal JG (2002) Release of annexin V-binding membrane microparticles from cultured human umbilical vein endothelial cells after treatment with camptothecin. BMC Cell Biol 3:11 Sims PJ, Faioni EM, Wiedmer T et al (1988) Complement proteins C5b-9 cause release of membrane vesicles from the platelet surface that are enriched in the membrane receptor for coagulation factor Va and express prothrombinase activity. J Biol Chem 263:18205–18212 Smalley DM, Ley K (2008) Plasma-derived microparticles for biomarker discovery. Clin Lab 54:67–79 Spees JL, Olson SD, Whitney MJ et al (2006) Mitochondrial transfer between cells can rescue aerobic respiration. Proc Natl Acad Sci USA 103:1283–1288 Stoorvogel W, Kleijmeer MJ, Geuze HJ et al (2002) The biogenesis and functions of exosomes. Traffic 3:321–330 Tailleux L, Pham-Thi N, Bergeron-Lafaurie A et al (2005) DC-SIGN induction in alveolar macrophages defines privileged target host cells for mycobacteria in patients with tuberculosis. PLoS Med 2:e381 Taranger CK, Noer A, Sorensen AL et al (2005) Induction of dedifferentiation, genomewide transcriptional programming, and epigenetic reprogramming by extracts of carcinoma and embryonic stem cells. Mol Biol Cell 16:5719–5735 Thery C, Boussac M, Veron P et al (2001) Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol 166:7309–7318 Tomas A, Yermen B, Min L et al (2006) Regulation of pancreatic β-cell insulin secretion by actin cytoskeleton remodelling: role of Gelsolin and cooperation with the MAPK signalling pathway. J Cell Sci 119:2156–2167 Valenti R, Huber V, Filipazzi P et al (2006) Human tumor-released microvesicles promote the differentiation of myeloid cells with transforming growth factor-beta-mediated suppressive activity on T lymphocytes. Cancer Res 66:9290–9298 Vandendries ER, Furie BC, Furie B (2004) Role of P-selectin and PSGL-1 in coagulation and thrombosis. Thromb Haemost 92:459–466 van Doormaal FF, Kleinjan A, Di Nisio M (2009) Cell-derived microvesicles and cancer. Neth J Med 67:266–273 VanWijk MJ, VanBavel E, Sturk A et al (2003) Microparticles in cardiovascular diseases. Cardiovasc Res 59:277–287 Whitlow MB, Klein LM (1997) Response of SCC-12F, a human squamous cell carcinoma cell line, to complement attack. J Invest Dermatol 109:39–45 Wolf P (1967) The nature and significance of platelet products in human plasma. Br J Haematol 13:269–288 Wysoczynski M, Ratajczak MZ (2009) Lung cancer secreted microvesicles: underappreciated modulators of microrenvironment in expanding tumors. Int J Cancer 125:1595–1603 Yingling JM, Blanchard KL, Sawyer JS (2004) Development of TGF-beta signalling inhibitors for cancer therapy. Nat Rev Drug Discov 3:1011–1022 Zwaal RF, Bevers EM (1983) Platelet phospholipid asymmetry and its significance in hemostasis. Subcell Biochem 9:299–334 Zwicker JI, Liebman HA, Neuberg D et al (2009) Tumor-derived tissue factor-bearing microparticles are associated with venous thromboembolic events in malignancy. Clin Cancer Res 15:6830–6840