PDF herunterladen
Semin Thromb Hemost 2013; 39(01): 033-039
DOI: 10.1055/s-0032-1333310
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Microparticles: New Protagonists in Pericellular and Intravascular Proteolysis

Romaric Lacroix
1   VRCM UMR_S1076, UFR de Pharmacie, Aix Marseille Université, INSERM, Marseille, France
2   Department of Hematology and Vascular Biology, Hôpital de la Conception, APHM, Marseille, France
,
Francoise Dignat-George
1   VRCM UMR_S1076, UFR de Pharmacie, Aix Marseille Université, INSERM, Marseille, France
2   Department of Hematology and Vascular Biology, Hôpital de la Conception, APHM, Marseille, France
› Institutsangaben
Weitere Informationen

Publikationsverlauf

Publikationsdatum:
09. Januar 2013 (online)

    Lizenzen und Reprints

Abstract

Microparticles (MPs) are small vesicles resulting from the shedding of cellular membrane during activation or apoptosis processes. Beyond their well-described procoagulant property, accumulating data show that specific endothelial cell-, leukocyte-, tumor-derived MPs bind plasminogen and vectorize plasminogen activators, leading to an efficient plasmin generation and matrix metalloproteinases activation. This review focuses on the molecular equipment of MPs subpopulations that identify MPs as efficient support for plasmin generation and the potential consequences of this new function. By the combined facts that MPs may disseminate, concentrate active proteolytic molecules and represent a protective environment against soluble inhibitors, MPs behave as an efficient catalytic surface involved in vascular and matrix proteolysis–related biological processes. The existence of this proteolytic MPs in the circulation or in body fluids raises the question about the physiological relevance of this activity. Consequences are suggested in many biological processes such as fibrinolysis, cell survival, matrix remodeling, angiogenesis, and tumor metastasis. However, further studies will be necessary to determine the extent in which in vivo MPs contribute to these pathophysiological mechanisms and how this circulating property of MPs may represent a new biomarker in specific clinical situations.

Keywords

microparticles - plasmin - matrix metalloproteinases - proteolysis
 

  • References

  • 1 Mathivanan S, Ji H, Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteomics 2010; 73 (10) 1907-1920
    CrossrefPubMedSuche in Google Scholar
  • 2 Hristov M, Erl W, Linder S, Weber PC. Apoptotic bodies from endothelial cells enhance the number and initiate the differentiation of human endothelial progenitor cells in vitro. Blood 2004; 104 (9) 2761-2766
    CrossrefPubMedSuche in Google Scholar
  • 3 Berda-Haddad Y, Robert S, Salers P , et al. Sterile inflammation of endothelial cell-derived apoptotic bodies is mediated by interleukin-1α. Proc Natl Acad Sci U S A 2011; 108 (51) 20684-20689
    CrossrefPubMedSuche in Google Scholar
  • 4 Morel O, Toti F, Jesel L, Freyssinet JM. Mechanisms of microparticle generation: on the trail of the mitochondrion!. Semin Thromb Hemost 2010; 36 (8) 833-844
    Thieme ConnectPubMedSuche in Google Scholar
  • 5 Hunter MP, Ismail N, Zhang X , et al. Detection of microRNA expression in human peripheral blood microvesicles. PLoS ONE 2008; 3 (11) e3694
    CrossrefPubMedSuche in Google Scholar
  • 6 Camussi G, Deregibus MC, Bruno S, Cantaluppi V, Biancone L. Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney Int 2010; 78 (9) 838-848
    CrossrefPubMedSuche in Google Scholar
  • 7 Owens III AP, Mackman N. Microparticles in hemostasis and thrombosis. Circ Res 2011; 108 (10) 1284-1297
    CrossrefPubMedSuche in Google Scholar
  • 8 Broze Jr GJ. Tissue factor pathway inhibitor. Thromb Haemost 1995; 74 (1) 90-93
    PubMedSuche in Google Scholar
  • 9 Kushak RI, Nestoridi E, Lambert J, Selig MK, Ingelfinger JR, Grabowski EF. Detached endothelial cells and microparticles as sources of tissue factor activity. Thromb Res 2005; 116 (5) 409-419
    CrossrefPubMedSuche in Google Scholar
  • 10 Aharon A, Katzenell S, Tamari T, Brenner B. Microparticles bearing tissue factor and tissue factor pathway inhibitor in gestational vascular complications. J Thromb Haemost 2009; 7 (6) 1047-1050
    CrossrefPubMedSuche in Google Scholar
  • 11 Steppich B, Mattisek C, Sobczyk D, Kastrati A, Schömig A, Ott I. Tissue factor pathway inhibitor on circulating microparticles in acute myocardial infarction. Thromb Haemost 2005; 93 (1) 35-39
    PubMedSuche in Google Scholar
  • 12 Tsimerman G, Roguin A, Bachar A, Melamed E, Brenner B, Aharon A. Involvement of microparticles in diabetic vascular complications. Thromb Haemost 2011; 106 (2) 310-321
    Thieme ConnectPubMedSuche in Google Scholar
  • 13 Pérez-Casal M, Downey C, Cutillas-Moreno B, Zuzel M, Fukudome K, Toh CH. Microparticle-associated endothelial protein C receptor and the induction of cytoprotective and anti-inflammatory effects. Haematologica 2009; 94 (3) 387-394
    CrossrefPubMedSuche in Google Scholar
  • 14 Pérez-Casal M, Downey C, Fukudome K, Marx G, Toh CH. Activated protein C induces the release of microparticle-associated endothelial protein C receptor. Blood 2005; 105 (4) 1515-1522
    CrossrefPubMedSuche in Google Scholar
  • 15 Rijken DC, Lijnen HR. New insights into the molecular mechanisms of the fibrinolytic system. J Thromb Haemost 2009; 7 (1) 4-13
    CrossrefPubMedSuche in Google Scholar
  • 16 Collen D. On the regulation and control of fibrinolysis. Edward Kowalski Memorial Lecture. Thromb Haemost 1980; 43 (2) 77-89
    PubMedSuche in Google Scholar
  • 17 Miles LA, Dahlberg CM, Plescia J, Felez J, Kato K, Plow EF. Role of cell-surface lysines in plasminogen binding to cells: identification of alpha-enolase as a candidate plasminogen receptor. Biochemistry 1991; 30 (6) 1682-1691
    CrossrefPubMedSuche in Google Scholar
  • 18 Hawley SB, Tamura T, Miles LA. Purification, cloning, and characterization of a profibrinolytic plasminogen-binding protein, TIP49a. J Biol Chem 2001; 276 (1) 179-186
    PubMedSuche in Google Scholar
  • 19 Pluskota E, Soloviev DA, Bdeir K, Cines DB, Plow EF. Integrin alphaMbeta2 orchestrates and accelerates plasminogen activation and fibrinolysis by neutrophils. J Biol Chem 2004; 279 (17) 18063-18072
    CrossrefPubMedSuche in Google Scholar
  • 20 Herren T, Burke TA, Das R, Plow EF. Identification of histone H2B as a regulated plasminogen receptor. Biochemistry 2006; 45 (31) 9463-9474
    CrossrefPubMedSuche in Google Scholar
  • 21 Lacroix R, Sabatier F, Mialhe A , et al. Activation of plasminogen into plasmin at the surface of endothelial microparticles: a mechanism that modulates angiogenic properties of endothelial progenitor cells in vitro. Blood 2007; 110 (7) 2432-2439
    CrossrefPubMedSuche in Google Scholar
  • 22 Toledo A, Coleman JL, Kuhlow CJ, Crowley JT, Benach JL. The enolase of Borrelia burgdorferi is a plasminogen receptor released in outer membrane vesicles. Infect Immun 2012; 80 (1) 359-368
    CrossrefPubMedSuche in Google Scholar
  • 23 Kwaan HC, Rego EM. Role of microparticles in the hemostatic dysfunction in acute promyelocytic leukemia. Semin Thromb Hemost 2010; 36 (8) 917-924
    Thieme ConnectPubMedSuche in Google Scholar
  • 24 Stein E, McMahon B, Kwaan H, Altman JK, Frankfurt O, Tallman MS. The coagulopathy of acute promyelocytic leukaemia revisited. Best Pract Res Clin Haematol 2009; 22 (1) 153-163
    CrossrefPubMedSuche in Google Scholar
  • 25 Angelucci A, D'Ascenzo S, Festuccia C , et al. Vesicle-associated urokinase plasminogen activator promotes invasion in prostate cancer cell lines. Clin Exp Metastasis 2000; 18 (2) 163-170
    CrossrefPubMedSuche in Google Scholar
  • 26 Dolo V, D'Ascenzo S, Violini S , et al. Matrix-degrading proteinases are shed in membrane vesicles by ovarian cancer cells in vivo and in vitro. Clin Exp Metastasis 1999; 17 (2) 131-140
    CrossrefPubMedSuche in Google Scholar
  • 27 Ginestra A, Miceli D, Dolo V, Romano FM, Vittorelli ML. Membrane vesicles in ovarian cancer fluids: a new potential marker. Anticancer Res 1999; 19 (4C) 3439-3445
    PubMedSuche in Google Scholar
  • 28 Ginestra A, Monea S, Seghezzi G , et al. Urokinase plasminogen activator and gelatinases are associated with membrane vesicles shed by human HT1080 fibrosarcoma cells. J Biol Chem 1997; 272 (27) 17216-17222
    CrossrefPubMedSuche in Google Scholar
  • 29 Graves LE, Ariztia EV, Navari JR, Matzel HJ, Stack MS, Fishman DA. Proinvasive properties of ovarian cancer ascites-derived membrane vesicles. Cancer Res 2004; 64 (19) 7045-7049
    CrossrefPubMedSuche in Google Scholar
  • 30 Brodsky SV, Malinowski K, Golightly M, Jesty J, Goligorsky MS. Plasminogen activator inhibitor-1 promotes formation of endothelial microparticles with procoagulant potential. Circulation 2002; 106 (18) 2372-2378
    CrossrefPubMedSuche in Google Scholar
  • 31 Lacroix R, Plawinski L, Robert S , et al. Leukocyte- and endothelial-derived microparticles: a circulating source for fibrinolysis. Haematologica 2012; 97 (12) 1864-1872
    CrossrefPubMedSuche in Google Scholar
  • 32 Rijken DC, Collen D. Purification and characterization of the plasminogen activator secreted by human melanoma cells in culture. J Biol Chem 1981; 256 (13) 7035-7041
    PubMedSuche in Google Scholar
  • 33 Pennica D, Holmes WE, Kohr WJ , et al. Cloning and expression of human tissue-type plasminogen activator cDNA in E. coli. Nature 1983; 301 (5897) 214-221
    CrossrefPubMedSuche in Google Scholar
  • 34 Rijken DC, Hoylaerts M, Collen D. Fibrinolytic properties of one-chain and two-chain human extrinsic (tissue-type) plasminogen activator. J Biol Chem 1982; 257 (6) 2920-2925
    PubMedSuche in Google Scholar
  • 35 Cesarman-Maus G, Hajjar KA. Molecular mechanisms of fibrinolysis. Br J Haematol 2005; 129 (3) 307-321
    CrossrefPubMedSuche in Google Scholar
  • 36 Millimaggi D, Festuccia C, Angelucci A , et al. Osteoblast-conditioned media stimulate membrane vesicle shedding in prostate cancer cells. Int J Oncol 2006; 28 (4) 909-914
    PubMedSuche in Google Scholar
  • 37 Dejouvencel T, Doeuvre L, Lacroix R , et al. Fibrinolytic cross-talk: a new mechanism for plasmin formation. Blood 2010; 115 (10) 2048-2056
    CrossrefPubMedSuche in Google Scholar
  • 38 Leroyer AS, Isobe H, Lesèche G , et al. Cellular origins and thrombogenic activity of microparticles isolated from human atherosclerotic plaques. J Am Coll Cardiol 2007; 49 (7) 772-777
    CrossrefPubMedSuche in Google Scholar
  • 39 Guller S, Tang Z, Ma YY, Di Santo S, Sager R, Schneider H. Protein composition of microparticles shed from human placenta during placental perfusion: Potential role in angiogenesis and fibrinolysis in preeclampsia. Placenta 2011; 32 (1) 63-69
    CrossrefPubMedSuche in Google Scholar
  • 40 Ramacciotti E, Hawley AE, Wrobleski SK , et al. Proteomics of microparticles after deep venous thrombosis. Thromb Res 2010; 125 (6) e269-e274
    CrossrefPubMedSuche in Google Scholar
  • 41 Ellis V, Murphy G. Cellular strategies for proteolytic targeting during migration and invasion. FEBS Lett 2001; 506 (1) 1-5
    CrossrefPubMedSuche in Google Scholar
  • 42 Plow EF, Herren T, Redlitz A, Miles LA, Hoover-Plow JL. The cell biology of the plasminogen system. FASEB J 1995; 9 (10) 939-945
    CrossrefPubMedSuche in Google Scholar
  • 43 Lijnen HR. Elements of the fibrinolytic system. Ann N Y Acad Sci 2001; 936: 226-236
    CrossrefPubMedSuche in Google Scholar
  • 44 Visse R, Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 2003; 92 (8) 827-839
    CrossrefPubMedSuche in Google Scholar
  • 45 Zucker S, Wieman JM, Lysik RM, Wilkie DP, Ramamurthy N, Lane B. Metastatic mouse melanoma cells release collagen-gelatin degrading metalloproteinases as components of shed membrane vesicles. Biochim Biophys Acta 1987; 924 (1) 225-237
    CrossrefPubMedSuche in Google Scholar
  • 46 Dolo V, Ginestra A, Ghersi G, Nagase H, Vittorelli ML. Human breast carcinoma cells cultured in the presence of serum shed membrane vesicles rich in gelatinolytic activities. J Submicrosc Cytol Pathol 1994; 26 (2) 173-180
    PubMedSuche in Google Scholar
  • 47 Dolo V, Ginestra A, Cassarà D , et al. Selective localization of matrix metalloproteinase 9, beta1 integrins, and human lymphocyte antigen class I molecules on membrane vesicles shed by 8701-BC breast carcinoma cells. Cancer Res 1998; 58 (19) 4468-4474
    PubMedSuche in Google Scholar
  • 48 Taraboletti G, D'Ascenzo S, Borsotti P, Giavazzi R, Pavan A, Dolo V. Shedding of the matrix metalloproteinases MMP-2, MMP-9, and MT1-MMP as membrane vesicle-associated components by endothelial cells. Am J Pathol 2002; 160 (2) 673-680
    CrossrefPubMedSuche in Google Scholar
  • 49 Lozito TP, Tuan RS. Endothelial cell microparticles act as centers of matrix metalloproteinsase-2 (MMP-2) activation and vascular matrix remodeling. J Cell Physiol 2012; 227 (2) 534-549
    CrossrefPubMedSuche in Google Scholar
  • 50 Aoki N, Jin-no S, Nakagawa Y , et al. Identification and characterization of microvesicles secreted by 3T3-L1 adipocytes: redox- and hormone-dependent induction of milk fat globule-epidermal growth factor 8-associated microvesicles. Endocrinology 2007; 148 (8) 3850-3862
    CrossrefPubMedSuche in Google Scholar
  • 51 Maeda S, Dean DD, Gay I, Schwartz Z, Boyan BD. Activation of latent transforming growth factor beta1 by stromelysin 1 in extracts of growth plate chondrocyte-derived matrix vesicles. J Bone Miner Res 2001; 16 (7) 1281-1290
    CrossrefPubMedSuche in Google Scholar
  • 52 Martínez de Lizarrondo S, Roncal C, Calvayrac O , et al. Synergistic effect of thrombin and CD40 ligand on endothelial matrix metalloproteinase-10 expression and microparticle generation in vitro and in vivo. Arterioscler Thromb Vasc Biol 2012; 32 (6) 1477-1487
    CrossrefPubMedSuche in Google Scholar
  • 53 Lacroix R, Dignat-George F. Microparticles as a circulating source of procoagulant and fibrinolytic activities in the circulation. Thromb Res 2012; 129 (Suppl. 02) S27-S29
    CrossrefPubMedSuche in Google Scholar
  • 54 Rossignol P, Luttun A, Martin-Ventura JL , et al. Plasminogen activation: a mediator of vascular smooth muscle cell apoptosis in atherosclerotic plaques. J Thromb Haemost 2006; 4 (3) 664-670
    CrossrefPubMedSuche in Google Scholar
  • 55 Meilhac O, Ho-Tin-Noé B, Houard X, Philippe M, Michel JB, Anglés-Cano E. Pericellular plasmin induces smooth muscle cell anoikis. FASEB J 2003; 17 (10) 1301-1303
    CrossrefPubMedSuche in Google Scholar
  • 56 Michel JB. Anoikis in the cardiovascular system: known and unknown extracellular mediators. Arterioscler Thromb Vasc Biol 2003; 23 (12) 2146-2154
    CrossrefPubMedSuche in Google Scholar
  • 57 Rossignol P, Ho-Tin-Noé B, Vranckx R , et al. Protease nexin-1 inhibits plasminogen activation-induced apoptosis of adherent cells. J Biol Chem 2004; 279 (11) 10346-10356
    CrossrefPubMedSuche in Google Scholar
  • 58 Doeuvre L, Plawinski L, Goux D, Vivien D, Anglés-Cano E. Plasmin on adherent cells: from microvesiculation to apoptosis. Biochem J 2010; 432 (2) 365-373
    CrossrefPubMedSuche in Google Scholar
  • 59 Tarui T, Majumdar M, Miles LA, Ruf W, Takada Y. Plasmin-induced migration of endothelial cells. A potential target for the anti-angiogenic action of angiostatin. J Biol Chem 2002; 277 (37) 33564-33570
    CrossrefPubMedSuche in Google Scholar
  • 60 Aoki N, Yokoyama R, Asai N , et al. Adipocyte-derived microvesicles are associated with multiple angiogenic factors and induce angiogenesis in vivo and in vitro. Endocrinology 2010; 151 (6) 2567-2576
    CrossrefPubMedSuche in Google Scholar
  • 61 McCready J, Sims JD, Chan D, Jay DG. Secretion of extracellular hsp90alpha via exosomes increases cancer cell motility: a role for plasminogen activation. BMC Cancer 2010; 10: 294
    CrossrefPubMedSuche in Google Scholar
  • 62 Jung T, Castellana D, Klingbeil P , et al. CD44v6 dependence of premetastatic niche preparation by exosomes. Neoplasia 2009; 11 (10) 1093-1105
    CrossrefPubMedSuche in Google Scholar