Semin Thromb Hemost 2013; 39(04): 329-337
DOI: 10.1055/s-0033-1334483
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Plasminogen Receptors: The First Quarter Century

Lindsey A. Miles
1   Department of Cell and Molecular Biology, The Scripps Research Institute, La Jolla, California
,
Robert J. Parmer
2   Department of Medicine, University of California San Diego, Veterans Administration San Diego Healthcare System, San Diego, California
› Author Affiliations
Further Information

Publication History

Publication Date:
26 March 2013 (online)

Abstract

The interaction of plasminogen with cell surfaces results in promotion of plasmin formation and retention on the cell surface. This results in arming cell surfaces with the broad-spectrum proteolytic activity of plasmin. Over the past quarter century, key functional consequences of the association of plasmin with the cell surface have been elucidated. Physiologic and pathophysiologic processes with plasmin-dependent cell migration as a central feature include inflammation, wound healing, oncogenesis, metastasis, myogenesis, and muscle regeneration. Cell surface plasmin also participates in neurite outgrowth and prohormone processing. Furthermore, plasmin-induced cell signaling also affects the functions of inflammatory cells, via production of cytokines, reactive oxygen species, and other mediators. Finally, plasminogen receptors regulate fibrinolysis. In this review, we highlight emerging data that shed light on longstanding controversies and raise new issues in the field. We focus on (1) the impact of the recent X-ray crystal structures of plasminogen and the development of antibodies that recognize cell-induced conformational changes in plasminogen on our understanding of the interaction of plasminogen with cells; (2) the relationship between apoptosis and plasminogen binding to cells; (3) the current status of our understanding of the molecular identity of plasminogen receptors and the discovery of a structurally unique novel plasminogen receptor, Plg-RKT; (4) the determinants of the interplay between distinct plasminogen receptors and cellular functions; and (5) new insights into the role of colocalization of plasminogen and plasminogen activator receptors on the cell surface.

 
  • References

  • 1 Miles LA, Plow EF. Binding and activation of plasminogen on the platelet surface. J Biol Chem 1985; 260 (7) 4303-4311
  • 2 Stricker RB, Wong D, Shiu DT, Reyes PT, Shuman MA. Activation of plasminogen by tissue plasminogen activator on normal and thrombasthenic platelets: effects on surface proteins and platelet aggregation. Blood 1986; 68 (1) 275-280
  • 3 Hajjar KA, Harpel PC, Jaffe EA, Nachman RL. Binding of plasminogen to cultured human endothelial cells. J Biol Chem 1986; 261 (25) 11656-11662
  • 4 Loscalzo J, Vaughan DE. Tissue plasminogen activator promotes platelet disaggregation in plasma. J Clin Invest 1987; 79 (6) 1749-1755
  • 5 Ellis V, Behrendt N, Danø K. Plasminogen activation by receptor-bound urokinase. A kinetic study with both cell-associated and isolated receptor. J Biol Chem 1991; 266 (19) 12752-12758
  • 6 Gonias SL, Braud LL, Geary WA, VandenBerg SR. Plasminogen binding to rat hepatocytes in primary culture and to thin slices of rat liver. Blood 1989; 74 (2) 729-736
  • 7 Duval-Jobe C, Parmely MJ. Regulation of plasminogen activation by human U937 promonocytic cells. J Biol Chem 1994; 269 (33) 21353-21357
  • 8 Félez J, Miles LA, Fábregas P, Jardí M, Plow EF, Lijnen RH. Characterization of cellular binding sites and interactive regions within reactants required for enhancement of plasminogen activation by tPA on the surface of leukocytic cells. Thromb Haemost 1996; 76 (4) 577-584
  • 9 Longstaff C, Merton RE, Fabregas P, Felez J. Characterization of cell-associated plasminogen activation catalyzed by urokinase-type plasminogen activator, but independent of urokinase receptor (uPAR, CD87). Blood 1999; 93 (11) 3839-3846
  • 10 Sinniger V, Merton RE, Fabregas P, Felez J, Longstaff C. Regulation of tissue plasminogen activator activity by cells. Domains responsible for binding and mechanism of stimulation. J Biol Chem 1999; 274 (18) 12414-12422
  • 11 Plow EF, Freaney DE, Plescia J, Miles LA. The plasminogen system and cell surfaces: evidence for plasminogen and urokinase receptors on the same cell type. J Cell Biol 1986; 103 (6 Pt 1) 2411-2420
  • 12 Hall SW, Humphries JE, Gonias SL. Inhibition of cell surface receptor-bound plasmin by alpha 2-antiplasmin and alpha 2-macroglobulin. J Biol Chem 1991; 266 (19) 12329-12336
  • 13 Miles LA, Plow EF. Receptor mediated binding of the fibrinolytic components, plasminogen and urokinase, to peripheral blood cells. Thromb Haemost 1987; 58 (3) 936-942
  • 14 Silverstein RL, Friedlander Jr RJ, Nicholas RL, Nachman RL. Binding of Lys-plasminogen to monocytes/macrophages. J Clin Invest 1988; 82 (6) 1948-1955
  • 15 Miles LA, Levin EG, Plescia J, Collen D, Plow EF. Plasminogen receptors, urokinase receptors, and their modulation on human endothelial cells. Blood 1988; 72 (2) 628-635
  • 16 Gonzalez-Gronow M, Gawdi G, Pizzo SV. Characterization of the plasminogen receptors of normal and rheumatoid arthritis human synovial fibroblasts. J Biol Chem 1994; 269 (6) 4360-4366
  • 17 Parmer RJ, Mahata M, Gong Y , et al. Processing of chromogranin A by plasmin provides a novel mechanism for regulating catecholamine secretion. J Clin Invest 2000; 106 (7) 907-915
  • 18 Jiang Q, Yasothornsrikul S, Taupenot L, Miles LA, Parmer RJ. The local chromaffin cell plasminogen/plasmin system and the regulation of catecholamine secretion. Ann N Y Acad Sci 2002; 971: 445-449
  • 19 Durliat M, Komano O, Correc P , et al. Plasminogen receptors on rat colon carcinoma cells. Br J Cancer 1992; 66 (1) 51-56
  • 20 Hembrough TA, Vasudevan J, Allietta MM, Glass II WF, Gonias SL. A cytokeratin 8-like protein with plasminogen-binding activity is present on the external surfaces of hepatocytes, HepG2 cells and breast carcinoma cell lines. J Cell Sci 1995; 108 (Pt 3) 1071-1082
  • 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
  • 22 Lacroix R, Plawinski L, Robert S , et al. Leukocyte- and endothelial-derived microparticles: a circulating source for fibrinolysis. Haematologica 2012; 97 (12) 1864-1872
  • 23 Bhattacharya S, Ploplis VA, Castellino FJ. Bacterial plasminogen receptors utilize host plasminogen system for effective invasion and dissemination. J Biomed Biotechnol 2012; 2012: 482096
  • 24 Sanderson-Smith ML, De Oliveira DM, Ranson M, McArthur JD. Bacterial plasminogen receptors: mediators of a multifaceted relationship. J Biomed Biotechnol 2012; 2012: 272148
  • 25 Ploplis VA, French EL, Carmeliet P, Collen D, Plow EF. Plasminogen deficiency differentially affects recruitment of inflammatory cell populations in mice. Blood 1998; 91 (6) 2005-2009
  • 26 Plow EF, Ploplis VA, Busuttil S, Carmeliet P, Collen D. A role of plasminogen in atherosclerosis and restenosis models in mice. Thromb Haemost 1999; 82 (Suppl. 01) 4-7
  • 27 Busuttil SJ, Ploplis VA, Castellino FJ, Tang L, Eaton JW, Plow EF. A central role for plasminogen in the inflammatory response to biomaterials. J Thromb Haemost 2004; 2 (10) 1798-1805
  • 28 Romer J, Bugge TH, Pyke C , et al. Impaired wound healing in mice with a disrupted plasminogen gene. Nat Med 1996; 2 (3) 287-292
  • 29 Creemers E, Cleutjens J, Smits J , et al. Disruption of the plasminogen gene in mice abolishes wound healing after myocardial infarction. Am J Pathol 2000; 156 (6) 1865-1873
  • 30 Madureira PA, Hill R, Miller VA, Giacomantonio C, Lee PW, Waisman DM. Annexin A2 is a novel cellular redox regulatory protein involved in tumorigenesis. Oncotarget 2011; 2 (12) 1075-1093
  • 31 Madureira PA, O'Connell PA, Surette AP, Miller VA, Waisman DM. The biochemistry and regulation of S100A10: a multifunctional plasminogen receptor involved in oncogenesis. J Biomed Biotechnol 2012; 2012: 353687
  • 32 Ranson M, Andronicos NM, O'Mullane MJ, Baker MS. Increased plasminogen binding is associated with metastatic breast cancer cells: differential expression of plasminogen binding proteins. Br J Cancer 1998; 77 (10) 1586-1597
  • 33 Palumbo JS, Talmage KE, Liu H, La Jeunesse CM, Witte DP, Degen JL. Plasminogen supports tumor growth through a fibrinogen-dependent mechanism linked to vascular patency. Blood 2003; 102 (8) 2819-2827
  • 34 Suelves M, López-Alemany R, Lluís F , et al. Plasmin activity is required for myogenesis in vitro and skeletal muscle regeneration in vivo. Blood 2002; 99 (8) 2835-2844
  • 35 López-Alemany R, Suelves M, Muñoz-Cánoves P. Plasmin generation dependent on alpha-enolase-type plasminogen receptor is required for myogenesis. Thromb Haemost 2003; 90 (4) 724-733
  • 36 Lopez-Alemany R, Suelves M, Diaz-Ramos A, Vidal B, Munoz-Canoves P. Alpha-enolase plasminogen receptor in myogenesis. Front Biosci 2005; 10: 30-36
  • 37 Jacovina AT, Zhong F, Khazanova E, Lev E, Deora AB, Hajjar KA. Neuritogenesis and the nerve growth factor-induced differentiation of PC-12 cells requires annexin II-mediated plasmin generation. J Biol Chem 2001; 276 (52) 49350-49358
  • 38 Gutiérrez-Fernández A, Gingles NA, Bai H, Castellino FJ, Parmer RJ, Miles LA. Plasminogen enhances neuritogenesis on laminin-1. J Neurosci 2009; 29 (40) 12393-12400
  • 39 Jiang Q, Taupenot L, Mahata SK , et al. Proteolytic cleavage of chromogranin A (CgA) by plasmin. Selective liberation of a specific bioactive CgA fragment that regulates catecholamine release. J Biol Chem 2001; 276 (27) 25022-25029
  • 40 Bai H, Nangia S, Parmer RJ. The plasminogen activation system and the regulation of catecholaminergic function. J Biomed Biotechnol 2012; 2012: 721657
  • 41 Syrovets T, Lunov O, Simmet T. Plasmin as a proinflammatory cell activator. J Leukoc Biol 2012; 92 (3) 509-519
  • 42 Li X, Syrovets T, Simmet T. The serine protease plasmin triggers expression of the CC-chemokine ligand 20 in dendritic cells via Akt/NF-κB-dependent pathways. J Biomed Biotechnol 2012; 2012: 186710
  • 43 Ling Q, Jacovina AT, Deora A , et al. Annexin II regulates fibrin homeostasis and neoangiogenesis in vivo. J Clin Invest 2004; 113 (1) 38-48
  • 44 Dassah M, Deora AB, He K, Hajjar KA. The endothelial cell annexin A2 system and vascular fibrinolysis. Gen Physiol Biophys 2009; 28(Spec No Focus): F20-F28
  • 45 Surette AP, Madureira PA, Phipps KD, Miller VA, Svenningsson P, Waisman DM. Regulation of fibrinolysis by S100A10 in vivo. Blood 2011; 118 (11) 3172-3181
  • 46 Madureira PA, Surette AP, Phipps KD, Taboski MA, Miller VA, Waisman DM. The role of the annexin A2 heterotetramer in vascular fibrinolysis. Blood 2011; 118 (18) 4789-4797
  • 47 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
  • 48 Law RH, Caradoc-Davies T, Cowieson N , et al. The X-ray crystal structure of full-length human plasminogen. Cell Rep 2012; 1 (3) 185-190
  • 49 Xue Y, Bodin C, Olsson K. Crystal structure of the native plasminogen reveals an activation-resistant compact conformation. J Thromb Haemost 2012; 10 (7) 1385-1396
  • 50 Miles LA, Dahlberg CM, Plow EF. The cell-binding domains of plasminogen and their function in plasma. J Biol Chem 1988; 263 (24) 11928-11934
  • 51 Castellino FJ, Ploplis VA. Structure and function of the plasminogen/plasmin system. Thromb Haemost 2005; 93 (4) 647-654
  • 52 Violand BN, Sodetz JM, Castellino FJ. The effect of epsilon-amino caproic acid on the gross conformation of plasminogen and plasmin. Arch Biochem Biophys 1975; 170 (1) 300-305
  • 53 Wiman B. Primary structure of peptides released during activation of human plasminogen by urokinase. Eur J Biochem 1973; 39 (1) 1-9
  • 54 Wiman B, Wallén P. Activation of human plasminogen by an insoluble derivative of urokinase. Structural changes of plasminogen in the course of activation to plasmin and demonstration of a possible intermediate compound. Eur J Biochem 1973; 36 (1) 25-31
  • 55 Violand BN, Castellino FJ. Mechanism of the urokinase-catalyzed activation of human plasminogen. J Biol Chem 1976; 251 (13) 3906-3912
  • 56 Han J, Baik N, Kim KH , et al. Monoclonal antibodies detect receptor-induced binding sites in Glu-plasminogen. Blood 2011; 118 (6) 1653-1662
  • 57 Félez J, Jardí M, Fàbregas P, Parmer RJ, Miles LA. Monoclonal antibodies against receptor-induced binding sites detect cell-bound plasminogen in blood. Blood 2012; 120 (3) 678-681
  • 58 Jardí M, Fàbregas P, Sagarra-Tió M, Pérez-Lucena MJ, Félez J. Characterization of plasminogen binding to NB4 promyelocytic cells using monoclonal antibodies against receptor-induced binding sites in cell-bound plasminogen. J Biomed Biotechnol 2012; 2012: 984589
  • 59 Dejouvencel T, Doeuvre L, Lacroix R , et al. Fibrinolytic cross-talk: a new mechanism for plasmin formation. Blood 2010; 115 (10) 2048-2056
  • 60 Gong Y, Kim S-O, Felez J, Grella DK, Castellino FJ, Miles LA. Conversion of Glu-plasminogen to Lys-plasminogen is necessary for optimal stimulation of plasminogen activation on the endothelial cell surface. J Biol Chem 2001; 276 (22) 19078-19083
  • 61 Miles LA, Castellino FJ, Gong Y. Critical role for conversion of glu-plasminogen to Lys-plasminogen for optimal stimulation of plasminogen activation on cell surfaces. Trends Cardiovasc Med 2003; 13 (1) 21-30
  • 62 Zhang L, Gong Y, Grella DK, Castellino FJ, Miles LA. Endogenous plasmin converts Glu-plasminogen to Lys-plasminogen on the monocytoid cell surface. J Thromb Haemost 2003; 1 (6) 1264-1270
  • 63 Thorsen S. The mechanism of plasminogen activation and the variability of the fibrin effector during tissue-type plasminogen activator-mediated fibrinolysis. Ann N Y Acad Sci 1992; 667: 52-63
  • 64 Marshall JM, Brown AJ, Ponting CP. Conformational studies of human plasminogen and plasminogen fragments: evidence for a novel third conformation of plasminogen. Biochemistry 1994; 33 (12) 3599-3606
  • 65 Hasumi K, Yamamichi S, Harada T. Small-molecule modulators of zymogen activation in the fibrinolytic and coagulation systems. FEBS J 2010; 277 (18) 3675-3687
  • 66 Tsirka SE, Bugge TH, Degen JL, Strickland S. Neuronal death in the central nervous system demonstrates a non-fibrin substrate for plasmin. Proc Natl Acad Sci U S A 1997; 94 (18) 9779-9781
  • 67 Chen ZL, Strickland S. Neuronal death in the hippocampus is promoted by plasmin-catalyzed degradation of laminin. Cell 1997; 91 (7) 917-925
  • 68 Houard X, Monnot C, Dive V, Corvol P, Pagano M. Vascular smooth muscle cells efficiently activate a new proteinase cascade involving plasminogen and fibronectin. J Cell Biochem 2003; 88 (6) 1188-1201
  • 69 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
  • 70 Zhang X, Chaudhry A, Chintala SK. Inhibition of plasminogen activation protects against ganglion cell loss in a mouse model of retinal damage. Mol Vis 2003; 9: 238-248
  • 71 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
  • 72 O'Mullane MJ, Baker MS. Loss of cell viability dramatically elevates cell surface plasminogen binding and activation. Exp Cell Res 1998; 242 (1) 153-164
  • 73 O'Mullane MJ, Baker MS. Elevated plasminogen receptor expression occurs as a degradative phase event in cellular apoptosis. Immunol Cell Biol 1999; 77 (3) 249-255
  • 74 Mitchell JW, Baik N, Castellino FJ, Miles LA. Plasminogen inhibits TNFalpha-induced apoptosis in monocytes. Blood 2006; 107 (11) 4383-4390
  • 75 Pluskota E, Soloviev DA, Szpak D, Weber C, Plow EF. Neutrophil apoptosis: selective regulation by different ligands of integrin alphaMbeta2. J Immunol 2008; 181 (5) 3609-3619
  • 76 Casar B, He Y, Iconomou M, Hooper JD, Quigley JP, Deryugina EI. Blocking of CDCP1 cleavage in vivo prevents Akt-dependent survival and inhibits metastatic colonization through PARP1-mediated apoptosis of cancer cells. Oncogene 2012; 31 (35) 3924-3938
  • 77 Deryugina EI, Quigley JP. Cell surface remodeling by plasmin: a new function for an old enzyme. J Biomed Biotechnol 2012; 2012: 564259
  • 78 Ranson M, Andronicos NM. Plasminogen binding and cancer: promises and pitfalls. Front Biosci 2003; 8: s294-s304
  • 79 Andronicos NM, Chen EI, Baik N , et al. Proteomics-based discovery of a novel, structurally unique, and developmentally regulated plasminogen receptor, Plg-RKT, a major regulator of cell surface plasminogen activation. Blood 2010; 115 (7) 1319-1330
  • 80 Wang GG, Calvo KR, Pasillas MP, Sykes DB, Häcker H, Kamps MP. Quantitative production of macrophages or neutrophils ex vivo using conditional Hoxb8. Nat Methods 2006; 3 (4) 287-293
  • 81 Félez J, Miles LA, Fábregas P, Jardí M, Plow EF, Lijnen RH. Characterization of cellular binding sites and interactive regions within reactants required for enhancement of plasminogen activation by tPA on the surface of leukocytic cells. Thromb Haemost 1996; 76 (4) 577-584
  • 82 Swaisgood CM, Schmitt D, Eaton D, Plow EF. In vivo regulation of plasminogen function by plasma carboxypeptidase B. J Clin Invest 2002; 110 (9) 1275-1282
  • 83 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
  • 84 Redlitz A, Fowler BJ, Plow EF, Miles LA. The role of an enolase-related molecule in plasminogen binding to cells. Eur J Biochem 1995; 227 (1–2) 407-415
  • 85 Hembrough TA, Kralovich KR, Li L, Gonias SL. Cytokeratin 8 released by breast carcinoma cells in vitro binds plasminogen and tissue-type plasminogen activator and promotes plasminogen activation. Biochem J 1996; 317 (Pt 3) 763-769
  • 86 Kassam G, Le BH, Choi KS , et al. The p11 subunit of the annexin II tetramer plays a key role in the stimulation of t-PA-dependent plasminogen activation. Biochemistry 1998; 37 (48) 16958-16966
  • 87 Choi KS, Fogg DK, Yoon CS, Waisman DM. p11 regulates extracellular plasmin production and invasiveness of HT1080 fibrosarcoma cells. FASEB J 2003; 17 (2) 235-246
  • 88 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
  • 89 Herren T, Burke TA, Das R, Plow EF. Identification of histone H2B as a regulated plasminogen receptor. Biochemistry 2006; 45 (31) 9463-9474
  • 90 Dudani AK, Ganz PR. Endothelial cell surface actin serves as a binding site for plasminogen, tissue plasminogen activator and lipoprotein(a). Br J Haematol 1996; 95 (1) 168-178
  • 91 Miles LA, Andronicos NM, Baik N, Parmer RJ. Cell-surface actin binds plasminogen and modulates neurotransmitter release from catecholaminergic cells. J Neurosci 2006; 26 (50) 13017-13024
  • 92 Hajjar KA, Jacovina AT, Chacko J. An endothelial cell receptor for plasminogen/tissue plasminogen activator. I. Identity with annexin II. J Biol Chem 1994; 269 (33) 21191-21197
  • 93 Fan ZQ, Larson PJ, Bognacki J , et al. Tissue factor regulates plasminogen binding and activation. Blood 1998; 91 (6) 1987-1998
  • 94 Miles LA, Dahlberg CM, Levin EG, Plow EF. Gangliosides interact directly with plasminogen and urokinase and may mediate binding of these fibrinolytic components to cells. Biochemistry 1989; 28 (24) 9337-9343
  • 95 Miles LA, Ginsberg MH, White JG, Plow EF. Plasminogen interacts with human platelets through two distinct mechanisms. J Clin Invest 1986; 77 (6) 2001-2009
  • 96 Gonzalez-Gronow M, Gawdi G, Pizzo SV. Plasminogen activation stimulates an increase in intracellular calcium in human synovial fibroblasts. J Biol Chem 1993; 268 (28) 20791-20795
  • 97 Lishko VK, Novokhatny VV, Yakubenko VP, Skomorovska-Prokvolit HV, Ugarova TP. Characterization of plasminogen as an adhesive ligand for integrins alphaMbeta2 (Mac-1) and alpha5beta1 (VLA-5). Blood 2004; 104 (3) 719-726
  • 98 Parkkinen J, Raulo E, Merenmies J , et al. Amphoterin, the 30-kDa protein in a family of HMG1-type polypeptides. Enhanced expression in transformed cells, leading edge localization, and interactions with plasminogen activation. J Biol Chem 1993; 268 (26) 19726-19738
  • 99 Kanalas JJ, Makker SP. Identification of the rat Heymann nephritis autoantigen (GP330) as a receptor site for plasminogen. J Biol Chem 1991; 266 (17) 10825-10829
  • 100 Kanalas JJ. Analysis of plasmin binding and urokinase activation of plasminogen bound to the Heymann nephritis autoantigen, gp330. Arch Biochem Biophys 1992; 299 (2) 255-260
  • 101 Eng JK, McCormick AL, Yates JRI. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J Am Soc Mass Spectrom 1994; 5: 976-989
  • 102 Miles LA, Lighvani S, Baik N , et al. The plasminogen receptor, Plg-R(KT), and macrophage function. J Biomed Biotechnol 2012; 2012: 250464
  • 103 Liu M, Zhang S. A kringle-containing protease with plasminogen-like activity in the basal chordate Branchiostoma belcheri . Biosci Rep 2009; 29 (6) 385-395
  • 104 Bai H, Baik N, Kiosses WB, Krajewski S, Miles LA, Parmer RJ. The novel plasminogen receptor, plasminogen receptor(KT) (Plg-R(KT)), regulates catecholamine release. J Biol Chem 2011; 286 (38) 33125-33133
  • 105 Miles LA, Andronicos NM, Chen EI , et al. Identification of the novel plasminogen receptor, Plg-RKT. In: Man TK, Flores RJ, , eds. Proteomics/Book 1: Human Diseases and Protein Functions. Rijeka, Croatia: Intech; 2012: 219-238
  • 106 Lighvani S, Baik N, Diggs JE, Khaldoyanidi S, Parmer RJ, Miles LA. Regulation of macrophage migration by a novel plasminogen receptor Plg-R KT. Blood 2011; 118 (20) 5622-5630
  • 107 Correc P, Fondanèche M-C, Bracke M, Burtin P. The presence of plasmin receptors on three mammary carcinoma MCF-7 sublines. Int J Cancer 1990; 46 (4) 745-750
  • 108 Miles LA, Hawley SB, Baik N, Andronicos NM, Castellino FJ, Parmer RJ. Plasminogen receptors: the sine qua non of cell surface plasminogen activation. Front Biosci 2005; 10: 1754-1762
  • 109 Plow EF, Doeuvre L, Das R. So many plasminogen receptors: why?. J Biomed Biotechnol 2012; 2012: 141806
  • 110 Das R, Burke T, Plow EF. Histone H2B as a functionally important plasminogen receptor on macrophages. Blood 2007; 110 (10) 3763-3772
  • 111 O'Connell PA, Surette AP, Liwski RS, Svenningsson P, Waisman DM. S100A10 regulates plasminogen-dependent macrophage invasion. Blood 2010; 116 (7) 1136-1146
  • 112 Gong Y, Hart E, Shchurin A, Hoover-Plow J. Inflammatory macrophage migration requires MMP-9 activation by plasminogen in mice. J Clin Invest 2008; 118 (9) 3012-3024
  • 113 Wygrecka M, Marsh LM, Morty RE , et al. Enolase-1 promotes plasminogen-mediated recruitment of monocytes to the acutely inflamed lung. Blood 2009; 113 (22) 5588-5598
  • 114 Rattner JB, Martin L, Waisman DM, Johnstone SA, Fritzler MJ. Autoantibodies to the centrosome (centriole) react with determinants present in the glycolytic enzyme enolase. J Immunol 1991; 146 (7) 2341-2344
  • 115 Ross M, Gerke V, Steinem C. Membrane composition affects the reversibility of annexin A2t binding to solid supported membranes: a QCM study. Biochemistry 2003; 42 (10) 3131-3141
  • 116 Das R, Plow EF. Phosphatidylserine as an anchor for plasminogen and its plasminogen receptor, histone H2B, to the macrophage surface. J Thromb Haemost 2011; 9 (2) 339-349
  • 117 Marguet D, Luciani MF, Moynault A, Williamson P, Chimini G. Engulfment of apoptotic cells involves the redistribution of membrane phosphatidylserine on phagocyte and prey. Nat Cell Biol 1999; 1 (7) 454-456
  • 118 Callahan MK, Halleck MS, Krahling S, Henderson AJ, Williamson P, Schlegel RA. Phosphatidylserine expression and phagocytosis of apoptotic thymocytes during differentiation of monocytic cells. J Leukoc Biol 2003; 74 (5) 846-856
  • 119 Zwaal RF, Comfurius P, Bevers EM. Surface exposure of phosphatidylserine in pathological cells. Cell Mol Life Sci 2005; 62 (9) 971-988
  • 120 Díaz-Ramos A, Roig-Borrellas A, García-Melero A, López-Alemany R. α-Enolase, a multifunctional protein: its role on pathophysiological situations. J Biomed Biotechnol 2012; 2012: 156795
  • 121 Simon DI, Rao NK, Xu H , et al. Mac-1 (CD11b/CD18) and the urokinase receptor (CD87) form a functional unit on monocytic cells. Blood 1996; 88 (8) 3185-3194
  • 122 Jiang YP, Pannell R, Liu JN, Gurewich V. Evidence for a novel binding protein to urokinase-type plasminogen activator in platelet membranes. Blood 1996; 87 (7) 2775-2781
  • 123 Felez J, Chanquia CJ, Fabregas P, Plow EF, Miles LA. Competition between plasminogen and tissue plasminogen activator for cellular binding sites. Blood 1993; 82 (8) 2433-2441
  • 124 Kassam G, Le BH, Choi KS , et al. The p11 subunit of the annexin II tetramer plays a key role in the stimulation of t-PA-dependent plasminogen activation. Biochemistry 1998; 37 (48) 16958-16966
  • 125 Fogg DK, Bridges DE, Cheung KK , et al. The p11 subunit of annexin II heterotetramer is regulated by basic carboxypeptidase. Biochemistry 2002; 41 (15) 4953-4961
  • 126 MacLeod TJ, Kwon M, Filipenko NR, Waisman DM. Phospholipid-associated annexin A2-S100A10 heterotetramer and its subunits: characterization of the interaction with tissue plasminogen activator, plasminogen, and plasmin. J Biol Chem 2003; 278 (28) 25577-25584